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Plant Growth

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Plants at SERC

Plants are vital to all life on Earth. They are important because plants take in carbon dioxide from the atmosphere and produce oxygen. In addition, plants make up the base of the food web by producing their own food using light, water, carbon dioxide, and other chemicals. This is why they are known as producers or Autotrophs . Examples of autotrophs on land are trees, vines, or shrubs. Autotrophs can also be found in the upper layers of the ocean, called algae. One of the many services autotrophs provide is to protect against erosion. Erosion is when the force of water, wind, or ice wash away layers of the soil that are necessary to protect against strong weather events like thunderstorms or hurricanes. If you lived on a hill that had little or no autotrophs and it rained really hard, over time, you would be at risk for landslides because their roots hold the soil together. Luckily, there are people who study plants, called botanists or plant ecologists/ scientists, and can tell us about why plants are needed! These scientists study the biology and chemistry of plants. In other words, they study the function of plants and why plants evolved the way they did, among other things. SERC has plant ecologists that study autotrophs and their interactions with other autotrophs, animals, and other living organisms. Read more about their research here: Plant Ecology at SERC .

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  • Photosynthesis is a chemical process that explains the way plants eat. It is also one of the processes that produce oxygen.
  • Frost date is the predicted day when it will be too cold to plant anything. This date is important to know because if it is too cold, your new plants will not do well so you have to wait until after this date to plant.
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  • Pollination is the transfer of pollen from one plant to another. This happens when pollen sticks to a pollinator such as a bee, bird, or bat while feeding on the nectar of a flower. 


  • Greenhouse gases , as stated by the Environmental Protection Agency (EPA) , are gases such as carbon dioxide and methane that trap heat in the Earth’s atmosphere. These greenhouse gases create the Greenhouse Effect which warms Earth’s surface (where we live) so we can live at a comfortable temperature.
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  • Review Paper
  • Open access
  • Published: 28 April 2021

The relationship between plant growth and water consumption: a history from the classical four elements to modern stable isotopes

  • Oliver Brendel   ORCID: 1  

Annals of Forest Science volume  78 , Article number:  47 ( 2021 ) Cite this article

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A Correction to this article was published on 17 June 2021

This article has been updated

Key message

The history of the relationship between plant growth and water consumption is retraced by following the progression of scientific thought through the centuries: from a purely philosophical question, to conceptual and methodological developments, towards a research interest in plant functioning and the interaction with the environment.

The relationship between plant growth and water consumption has for a long time occupied the minds of philosophers and natural scientists. The ratio between biomass accumulation and water consumption is known as water use efficiency and is widely relevant today in fields as diverse as plant improvement, forest ecology and climate change. Defined at scales varying from single leaf physiology to whole plants, it shows how botanical investigations changed through time, generally in tandem with developing disciplines and improving methods. The history started as a purely philosophical question by Greek philosophers of how plants grow, progressed through thought and actual experiments, towards an interest in the functioning of plants and the relationship to the environment.

This article retraces this history by following the progression of scientific questions posed through the centuries, and presents not only the main methodological and conceptual developments on biomass growth and transpiration but also the development of the carbon isotopic method of estimation. The history of research on photosynthesis is only touched briefly, but the development of research on transpiration and stomatal conductance is presented with more detail.

Research on water use efficiency, following a path from the whole plant to leaf-level functioning, was strongly involved in the historical development of the discipline of plant ecophysiology and is still a very active research field across nearly all levels of botanical research.

1 Introduction

The ratio of biomass accumulation per unit water consumption is known today as water use efficiency (WUE) and is widely relevant to agriculture (e.g. Blum 2009 ; Tallec et al. 2013 ; Vadez et al. 2014 ), to forest ecology (e.g. Linares and Camarero 2012 ; Lévesque et al. 2014 ) and in the context of global climate change (Cernusak et al. 2019 ). This ratio can be defined at various levels, from the physiological functioning of a leaf to the whole plant and at the ecosystem level. This historical review starts at the whole plant level, where WUE can be simply measured by quantifying the amount of water given to a plant and the plant’s increase in biomass during the experiment. The ratio of biomass produced divided by the cumulative water lost during growth is termed whole plant transpiration efficiency (TE= biomass produced/water lost). Historically, the ratio has also been calculated in its inverted form (water lost/biomass produced) and various terms have been used to denote these ratios (see Box 1). As knowledge, concepts and technology advanced, it became desirable to measure TE also at the leaf level, where it is defined either as the ratio of net CO 2 assimilation rate to transpiration (or to the stomatal conductance for water vapour). Therefore, some history of the two leaf-level components of WUE is included here. Numerous articles have been published on the history of the development of research on photosynthesis, and other than the reviews cited in this article, the publications by Govindjee are notable, especially Govindjee and Krogmann ( 2004 ), as they include a long list of other writings on the history of photosynthesis. On the other hand, little has been written about the history of research on transpiration and stomatal conductance. Notable is Brown ( 2013 ), who wrote specifically on the cohesion-tension theory of the rise of sap in trees, including many writings from the late nineteenth century. Consequently, here, photosynthesis research is only broached briefly, whereas transpiration research is more detailed.

As the development of the research on WUE spans a very long period, starting with Greek philosophers, publications are in several languages. Classical writings were in Greek or in Latin, and for these translations are available. However, from the mid-seventeenth century onwards, national languages were more and more used, which can be seen in the number of French- and German-language publications. This review is also a tribute to these nowadays less known seventeenth, eighteenth and nineteenth century French and German natural philosophers and their contribution to the development of the science of plant ecophysiology. Also, towards the beginning of the twentieth century, publications became too numerous to allow a comprehensive review; thus, the author focussed on the use of the carbon stable isotopes methodology and on tree ecology.

Box 1 Short history of names for whole plant transpiration efficiency (TE)

2 what is plant matter made of.

Various Greek philosophers were interested in how substances can change from one thing into another. Thales (624–c. 546 BC) thought that all things come from water, whereas Anaximenes argued that “pneuma” (air) should be the basis of all things (Egerton 2001a ). These assertions were the basis of more than 2000 years of philosophical dispute.

In “De Causis Plantarum”, Theophrastos (371–287 BC) assumed that plants draw nutrition, which consisted of varying amounts of the four elementary humours, from the earth through their roots (Morton 1981 ). Some centuries later, in a Christian work translated in 400 AD from Greek into Latin and known as “Pseudo-Clement’s Recognitions”, an apparent thought experiment was described to “prove that nothing is supplied to seeds from the substance of the earth, but that they are entirely derived from the element of water and the spirit (spiritus) that is in it” (Egerton 2004c ). The author of this thought experiment suggested putting earth into big barrels, growing herbaceous plants in it for several years, then harvesting them and weighing them. His hypothesis was that the weight of the earth would not have changed, and the author used this as an argument that the vegetation biomass could have come only from water. This thought experiment revealed a progress in scientific thinking because the question was posed more precisely than before. It stood out at a time when botany mainly consisted of naming plants and “theoretical botany effectually went out of existence” (Morton 1981 ).

It appears that the question of how plant matter is produced was not pursued in Roman or Arabic writings, which were more concerned with agricultural (the former) and medical (the latter) aspects of plant sciences (Egerton 2001b , 2002 ). Not until the High Middle Ages was a renewed interest shown in plant growth. Adelard of Bath, a twelfth century English natural philosopher, devoted the first four chapters of “Questiones Naturales” (c. 1130–1140; Morton 1981 ) to the question of what plant matter is made of. He argued, within the concepts of the four elements theory, “by just as much as water differs from earth, by so much does it afford less nourishment to roots, I mean than earth does”, clearly being in favour of earth as the source for plant nourishment. His arguments were only theoretical and speculative.

A major step occurred in botanical sciences between the fifteenth and sixteenth centuries; scholars began making experiments to test antique and medieval hypotheses against observations in nature (Egerton 2003 ). In the mid-fifteenth century, and probably related to the translation and printing of the botanical books by Theophrastus (Morton 1981 ), the thought experiment from “Recognitions...” was taken up by Nicholas of Cusa in the fourth part of his “Idiota de mente”, “De staticis experiments”. At a time when the naming of plants for pharmacology was the major interest of savants, he proposed experimental investigations. Nicholas of Cusa described the same thought experiment as did Pseudo-Clement’s Recognitions ; he concluded similarly that “the collected herbs have weight mainly from water” (1450; translation into English by Hopkins 1996 ). Cusa additionally suggested that the plants should be burned at the end of the experiment and the ash weight be taken into account. It is not clear whether the thought experiment was ever physically done.

In the sixteenth century, botanical science began to separate from medical sciences, with the establishment of lectureships in universities (e.g. Padua in 1533) and the establishment of botanical gardens (Egerton 2003 ). The bases existed for advancing science in the seventeenth century of Enlightenment. Francis Bacon, an influential philosopher of his time, conducted a series of plant growth experiments which are reported in his “de Augmentis Scientiarum” (1623; Spedding et al. 1900 ). Bacon discovered that some plants sprouted more quickly in water than in soil (Egerton 2004b ). He concluded that “for nourishment the water is almost all in all, and that the earth doth but keep the plant upright, and save it from over-heat and over-cold” (Hershey 2003 ), thus still upholding the theory proposed by Thales and Nicholas of Cusa. In “The History of the Propagation and Improvement of Vegetable”, Robert Sharrock ( 1660 ) reported that some plants both rooted and grew entirely in water. Although he noted different amounts of transpiration over time, he did not discuss this in relation to plant growth.

In 1662, Johannes Baptista van Helmont published his now-famous willow experiments (van Helmont 1662 ). This may be the first report of an experiment that was based on the thought experiment of Nicholas of Cusa (Hershey 2003 ) with the minor differences of beginning with dried soil and not using herbaceous plants, but rather a willow tree. After weighing the soil, he irrigated it with rain water and planted the weighed stem of a willow tree. The experiment ran for 5 years. At the end, the tree was weighed again, as was the dried soil. He found the soil weighed about 2 ounces less than at the beginning of the experiment, whereas 164 pounds of wood, bark and roots was produced. He concluded that the organic matter could only have come out of the water. Helmont was unaware of the existence of carbon dioxide, but he did know of “gas sylvestre”. He also knew that burning oak charcoal would produce nearly the same amount of gas sylvestre and ash. However, he did not connect this information with the plant growth he had observed (Hershey 2003 ). Robert Boyle published similar experiments in “The sceptical Chymist” (Boyle 1661 ). Boyle claimed that he had done his experiments before he knew of Helmont’s (Egerton 2004c ), although he discussed Helmont’s results and arguments in detail in his book. Boyle doubted the direct transformation of water into plant matter. He admitted, however, that it might be possible that other substances contained in the water could generate new matter (Boyle 1661 ). In the 1660’s, Edme Mariotte also criticised van Helmont’s theory that water alone constituted the only element to produce plant matter. He thought similarly to Boyle that elements in the water could contribute to the plant matter. He also showed that nitrogen compounds were important for plant growth (Bugler 1950 ).

John Woodward, in his “Some Thoughts and Experiments Concerning Vegetation” (Woodward 1699 ), took up again the question of what comprised the source of plant growth. Woodward criticised Helmont’s and Boyle’s experiments, mainly on the precision of weighing the dry soil before and after the experiment, but also the contamination of the irrigation water by terrestrial vegetable or mineral matter. Consequently, he developed a series of hydroponics experiments, where by growing plants in sealed vials, in different types of water and weighing them regularly over the same time period, he could calculate how much biomass was gained over a set time period. He was able to draw a series of conclusions from these experiments by calculating the ratio of water lost to plant mass gained in the same period of time, thereby calculating the inverse of transpiration efficiency. This was probably the first time that the inverse of transpiration efficiency was calculated using experimental data. He showed that 50 to 700 times as much water was lost than biomass gained. He also reported that plants grown in water containing more terrestrial matter grew more and with less water consumed. From these observations, he concluded that water serves only as a vehicle for the terrestrial matter that forms vegetables and that vegetable matter is not formed out of water. He is still remembered more for his geological publications (Porter 1979 ) than for his contributions to botany (Stanhill 1986 ).

In his “history of ecology” series, Egerton ( 2004c ) nicely sums this period thusly: “each of these authors (Bacon, Boyle, Helmont, Sharrock) built upon the work of his predecessors and improved somewhat the understanding of plant growth and how to study it. However, they still fell short of a basic understanding of plant growth. Before that could be achieved, chemists would have to identify the gases in the air”. This series of studies shows that from the end of the seventeenth century onwards, experiments replaced speculation (Morton 1981 ), in botany as well as in many other areas of science.

From the end of the seventeenth century, the question of how plants grow was still unresolved, although it was known that nutrients were conducted from the roots in the ascending sap to the leaves. A major improvement in the understanding of how transpiration and its variations work was the discovery of cells by Robert Hooke towards the middle of the seventeenth century (Egerton 2005 ) and subsequently the discovery of stomata on leaf surfaces. One of the first to describe stomata may have been Malpighi in “Anatomy of Plants” (Malpighi 1675 in Möbius 1901 ). Based on Malpighi’s and Grew’s ( 1682 ) studies, John Ray suggested in “Historia Plantarum” (Ray 1686 in Lazenby 1995 ) that the apertures in the leaves, when open, would give off either breath or liquid. Ray may have been the first to have connected stomata with transpiration. He also suggested that the loss of water by evaporation is compensated constantly by water from the stem, and thus transpiration results from a constant water flux. He also observed that sap ascends the stems of trees in sap-bearing vessels which do not contain valves. He did, however, admit that it cannot be capillary forces that make water go up tall trees.

Ideas on photosynthesis developed slowly from the middle of the seventeenth century onwards. Malpighi ( 1675 ) suggested that leaves produce (“concoct and prepare”) the food of plants and from leaves this food passes to all parts of the plant. Similarly, Claude Perrault in “Essais de Physique” (Perrault 1680 ) defended the hypothesis that the root acts as the mouth of the plant and that the leaves serve to prepare the food arriving with the sap from the root so that it can be used in the rest of the plant. John Ray in “History Plantarum” (Ray 1686 in Lazenby 1995 ) concurs with this, however adding in “The wisdom of God” (Ray 1691 in Lazenby 1995 ) that “not only that which ascends from the Root, but that which they take in from without, from the Dew, moist Air, and Rain”. He also thought that light could play a role in this preparation of the plant sap. At this time, most authors (Malpighi, Perrault, Mariotte, Ray) knew about the circulation of sap, up as well as down, and that leaves served somehow to transform the upcoming sap into food for the plant.

In 1770 , Lavoisier published “Sur la nature de l’eau” (“On the nature of water”, translation by the author) and reviewed the literature on the possibility of water changing into earth to nourish plants. Lavoisier cited the Van Helmont experiment and later works which tested Van Helmont’s idea by growing plants in water (e.g. Boyle, however he did not cite Woodward). He was critical of the idea that it could be a transformation of water that would constitute plant material. This was based mainly on experiments by himself and others, showing even distilled water would contain traces of “soil”. However, he also defended the idea, based mainly on Charles Bonnet’s observations, that leaves absorb vapours from the atmosphere that contribute to plant growth.

Helmont had coined the term “gaz” in the mid-seventeenth century and had been able to distinguish different gazes from air (Egerton 2004a ). It was only in the middle of the eighteenth century that gases were studied in the laboratory and several observations by different researchers would finally lead to an understanding of respiration and photosynthesis (Tomic et al. 2005 ; Nickelsen 2007 ). Richard Bradley seems to be one of the first to clearly state (in letters from 1721 to 1724) that plant nourishment can be drawn from the air. Hales ( 1727 ) agreed with this theory, which was not yet widely accepted (Morton 1981 ), and suggested that light might be involved, which helped to pave the way for the discovery of photosynthesis. Black ( 1756 ) was able to identify carbon dioxide (which he called fixed air) using a lime water precipitation test. He demonstrated that this “fixed air” did not support animal life or a candle flame (Egerton 2008 ). Charles Bonnet ( 1754 ) made an important observation, i.e. branches with leaves that were submerged under water would produce air bubbles on their surfaces when sunlight shone on them, but not after sunset. Senebier refined these experiments in 1781 (Morton 1981 ), by showing that the leaves produced no oxygen in the sunlight when the surrounding water was free of carbon dioxide and that the rate of oxygen production was higher with carbon dioxide-saturated water. Tomic et al. ( 2005 ) present nicely the steps leading up to the term photosynthesis. This began with Priestley ( 1775 ) demonstrating that the air given off by animals and by plants was not the same, Ingen-Housz ( 1779 ) observed the important role of light, and the dispute between Senebier and Ingen-Housz from 1783 to 1789 resolved more clearly the functions of carbon dioxide emission (respiration) and absorption (photosynthesis). Based on these results and his own very detailed observations, de Saussure reported in 1804 that the carbon necessary for plant growth is absorbed mainly by green leaves from atmospheric carbon dioxide and he estimated that the largest part of the accumulated dry matter of plants is made of this carbon. Thus, the dispute of what the plant matter is made of that began in antique Greece was resolved at the end of the eighteenth century.

3 How much water do plants need to grow?

The late eighteenth century marked the beginning of applied agricultural science and the rise of plant physiology (Morton 1981 ). Work continued on transpiration and stomata, with a large number of experiments. Burgerstein ( 1887 , 1889 ) managed to assemble 236 publications on transpiration of plants from 1672 to 1886, citing short abstracts of each and comparing them critically. Also, Unger published in 1862 a major review article covering such subjects as the relationship of transpiration to temperature and humidity; daily cycles, including night; differences in adaxial and abaxial leaf surfaces; the impact on transpiration of type, number, size and distribution of stomata; the structure of the epidermis (cell layers, cuticle, hairs and wax); development of the mesophyll; size of intercellular spaces and cell turgor; and the impact of plant transpiration on the atmosphere (Unger 1862 in Burgerstein 1887 ). Scientists started to reflect on the interaction of plants, or more specifically their leaves, with their environment, and experimentation included the responses of stomata to light quantity (Möldenhawer 1812 ) and quality (Daubeny 1836 in Burgerstein 1887 ). Based on inconsistent observations by e.g. Banks, Möldenhawer and Amici, advances were also made on the functioning of stomata (Mohl 1856 ). However, progress was mainly based on a comment in von Schleiden ( 1849 ) that the state of the stomata would be the result of the water in- or outflow of the pore cells (called “Schliesszellen”) and he showed experimentally that stomata close when the pore cells lose water. As knowledge of transpiration, stomatal opening and their dependence on environmental variables increased, new questions arose about the water consumption of plants.

Another milestone along the way to understanding the transpiration of plants in the nineteenth century was the publication by Sir John Bennet Lawes ( 1850 ), “Experimental investigation into the amount of water given off by plants during their growth; especially in relation to the fixation and source of their various constituents”. He described experiments on wheat, barley, beans, peas and clover using differently fertilised soils. He was using plants in closed containers and an especially designed balance to “estimate the amounts of water given off” (Fig. 1 ). He observed increased evapotranspiration with higher temperatures during the growing season, and asked whether “this increased passage of water through the plants, carrying with it in its course many important materials of growth from the soil, and probably also influencing the changes in the leaves of these, as well as of those derived from the atmosphere, will not be accompanied with an equivalently increased growth and development of the substance of the plant”. This was followed by an important discussion of the influence of temperature on evaporation and growth as well as the resultant ratio. He discussed in the introduction “the relationship of the water given off to the matter fixed in the plants”; he gave his results in this ratio and in the inverse ratio, and applied these ratios to different scientific questions. The first ratio (transpired water divided by plant matter, the inverse of today’s TE) was used to interpret his results in terms of water use compared to field available water, and the latter’s ratio (plant matter divided by transpired water, equivalent to today’s TE) was used to discuss his results in terms of functional differences among species. From the observed functional differences, he concluded that there was “some definite relationship between the passage of water through the plants and the fixation in it of some of its constituents”. He was, thereby, introducing a new question about the link between dry matter accumulation and transpiration, which will be treated in the next chapter.

figure 1

Illustration from Lawes ( 1850 , p. 43) of the special balance constructed for weighing plants in their “jars” to estimate the amounts of water given off and also the “truck” on which a series of jars was moved to the balance

Towards the end of the nineteenth century, research interest started to include agricultural questions of water use. Marié-Davy ( 1869 ) measured transpiration (standardised by leaf surface) of over 30 plant species, including eight tree or shrub species as well as herbaceous and agricultural plants. He estimated transpiration per soil area, thereby establishing that a prairie would transpire more than trees. von Höhnel ( 1879 ) estimated long-term transpiration of branches of 15 tree species (standardised on leaf surface or leaf dry weight). He used these data of branch transpiration to upscale to whole trees and concluded that compared to agricultural plants, the amount of rain seemed sufficient for tree growth. Hellriegel ( 1871 ) had already similarly concluded for cereals in the Mark Brandenburg (Germany) region that rainfall would not be sufficient, as had Marié-Davy ( 1874 ) for wheat in the Paris (France) region. In parallel with these more quantitative interrogations about water use, from the mid-nineteenth century, scientists started to ask more functional questions about the relationship between transpiration and dry matter accumulation, in a context of vigorous growth of botanical sciences and the complex relation between organisms and their environment (Morton 1981 ).

4 Are transpiration and dry matter accumulation linked?

Lawes ( 1850 ) had already reflected on a functional relationship between water flux and plant matter accumulation. In the following years, there were several publications on the transpiration of trees, and although no transpiration efficiency was estimated, the understanding of tree transpiration advanced. Many comparative studies were published. Lawes ( 1851 ) on “Comparative evaporating properties of evergreen and deciduous trees” considered twelve different tree species. He provided measurements of the variation in transpiration with temperature and hygrometry data. With these, he concluded that “evaporation is not a mere index of temperature but that it depends on vitality influenced by heat, light and other causes”. In the late nineteenth century, several researchers estimated and compared values of the ratio of transpiration and dry matter accumulation for different plants (Burgerstein 1887 ). With the growing evidence of variation in this ratio, scientists started to reflect on the relationship between transpiration and dry matter accumulation, aided by the development of new measurement techniques. A major question was if there would be a tight coupling between transpiration and dry matter accumulation, resulting in a constant transpiration efficiency, or if variation could be observed.

Dehérain ( 1869 ) studied evaporation and the decomposition of carbonic acid in leaves of wheat and barley. Using an ingenious apparatus, he was probably the first to directly measure evaporation of water in parallel with carbonic acid decomposition. He studied the effect of variously coloured light, and although he did not calculate the ratio between evaporation and carbonic acid decomposition, he did conclude that light of different colours had a similar effect on carbonic acid decomposition and on water evaporation from the leaves. His final conclusion was that “it is likely that there is existing between the two main functions of plants, evaporation and carbonic acid decomposition, a link, of which we need to determine its nature” (translation from the original French by the author). Several other scientists also commented on the relationship between transpiration and dry matter production. Fittbogen ( 1871 ) supposed, similarly to Lawes ( 1850 ) before him, but with more experimental evidence, that there should be a positive relationship between transpiration and production of dry matter. Dietrich ( 1872 in Burgerstein 1887 ) supposed that this relationship would be linear, whereas Tschaplowitz ( 1878 in Burgerstein 1887 ) introduced the idea that there should be an optimum transpiration at the maximum production of matter. Therefore, when the transpiration would increase over this optimum, this would lead to a decrease in assimilation rate. He was one of the first to suggest a non-linear relationship between transpiration and assimilation. Sorauer in “Studies on evaporation” ( 1880 ) defended the hypothesis that transpiration was not only a physical phenomenon but was also physiological. He stated that “It is not possible as yet to study the plant internal processes which regulate the transpiration, however it is possible to quantify the relationship between dry-matter and transpiration” (translation from German by the author), suggesting thereby TE as a means to advance the understanding of plant internal processes. Sorauer was probably at the cutting edge of science of his time. He pointed out specifically that variability among plants of one species was due to genetics (German, “erbliche Anlagen”), a startling and even daring assertion for his time. He asserted that for comparative studies, genetic variability needed to be minimised. To achieve this, he used, when possible, seeds from the same mother plant, grown in the same environmental conditions and a large number of repetitions. Using these protocols, he was probably one of the first to estimate TE on tree seedlings, showing that there was within species diversity in transpiration and growth, but that their ratio was more constant. He concluded from experiments on pear and apple trees that the pear trees used less water for the same biomass growth. He was able to go one step further and demonstrate that this difference was due to less transpiration per leaf area. By comparing different woody and herbaceous plants with different growth types, he postulated that when plants had a small leaf area combined with high transpiration, they had either a very strong growth increment, a high dry matter percentage, or a large root system. Overall, he observed relationships between dry matter production and transpiration; he concluded that there must be some regulation of the transpiration per unit leaf area by the co-occurring dry matter production.

Hellriegel ( 1883 ) argued that one cannot estimate a constant ratio between transpiration and production as there were factors which influence each independently. He also commented that it might make sense to estimate mean values of transpiration for various agricultural plants, as this would be for practical and scientific value. He thought that the most logical standardisation would be by the mass of the dry matter produced during the same time period. He called this “relative Verdunstungsgrösse” which can be translated into English as “relative transpiration”. He was probably one of the first to give a name to the ratio between whole plant transpiration and dry matter production. He proposed a theory that for a long-term drought, plants would acclimate their morphology to decrease their “relative transpiration”. He provided additional experimental evidence that barley had decreased in relative transpiration over as many as seven levels of soil water deficit, relative to field capacity. Using his own observations, he proposed that when calculating a mean “relative transpiration” for a single species, variation of transpiration should be minimised and that plants should be tested together only under optimal conditions. Given the relatively small differences in relative transpiration that he observed among different crops, Hellriegel suggested that these differences would not explain why some crops grow better in wet locations and others on dry locations. Hellriegel was thus probably one of the first scientists to point out that the relationship between drought adaptation and “relative transpiration” might not be straightforward.

Understanding how biomass and water loss were connected was studied by Iljin ( 1916 ) on a newly detailed level. He measured simultaneously water loss and carbon dioxide decomposition and reported his data as grammes of water lost per cubic centimetre of carbon dioxide decomposed. He concluded from studying more than 20 plant species that “ is generally agreed that the rates of water loss and of CO 2 assimilation are directly proportionate to stomatal aperture, and that consequently there exists a close connection between these two processes”.

At the end of the nineteenth century, the ratio of transpiration versus dry matter accumulation was recognised as an important plant trait, which varies among and within species in a complex interaction of each component with the other and with environmental factors.

5 How do plants differ in water requirement and how do they respond to variations in environmental factors?

In the late nineteenth century, several researchers estimated and compared values of the ratio of transpiration and dry matter accumulation for a range of cultivated plants (Fittbogen 1871 ; Dietrich 1872 ; Farsky 1877 , cited in Burgerstein 1887 ), giving evidence of the growing interest of agricultural scientists. The number of studies of transpiration efficiency greatly increased, thereby driving a new standardisation in terminology. King ( 1889 ) studied the inverse of transpiration efficiency and described it as “the amount of water required for a ton of dry matter”, and promulgated this terminology by using it in the titles of his publications between 1892 and 1895. Similarly, Leather ( 1910 ) published “Water requirements of the crops of India”, in which he defined the “transpiration ratio” as “the water transpired to the weight of dry plant produced”. The shift from a purely descriptive use of “water requirement” to a clearly defined one was provided by Kearney and Shantz ( 1911 ) as “… the degree to which a plant is economical in its use of water is expressed in its water requirement, or the total quantity of water which it expends in producing a pound of dry matter”. The term “water requirement” is the inverse of the modern transpiration efficiency, and was used by a rapidly increasing number of publications which were published on the water use of crops in the early twentieth century. Montgomery ( 1911 ) may have been the first to use the term for a plant trait in “Methods of determining the water requirements of crops”.

At the beginning of the twentieth century, the importance of gaining knowledge on the water requirements of plants can be seen in the technical effort that went into the measuring equipment. von Seelhorst ( 1902 ) presented a system of growing boxes on rails, placed belowground, including the balance, so that the top of the growing boxes was at the same level as the surrounding soil (Fig. 2 ). In the now well-known studies on “The water requirement of plants. I. Investigations in the Great Plains in 1910 and 1911”, Briggs and Shantz ( 1913a ) measured the water requirement for 21 crop and weed species, sometimes for different varieties of the same crop and under controlled and field conditions. In the same year, they reviewed the available literature on water requirement (Briggs and Shantz 1913b ), increasing their dataset to 31 different crop species. They discussed in detail studies from 29 different authors, many of which had only published once or twice on this subject. A few researchers were notable for their number of publications on the water requirement of crop plants: King with 6 publications between 1889 and 1905, and von Seelhorst with 9 publications between 1899 and 1907. The largest contributions came from Hellriegel ( 1883 ; 10 species) and Leather ( 1911 ; 15 species). Kiesselbach ( 1916 ) also reviewed 59 publications from 1850 to 1915 “which had studied transpiration in relation to crop yield, based upon plants grown beyond the seedling stage”. There were regular publications of original work from 1870s onwards, with more than one publication per year from 1890 onwards. The difference among species and the impact of environmental factors on water requirement was one of the main questions raised. These reviews and the increasing amount of newly published work per year are evidence of the growing interest in the “water requirement” of plants as a trait of increasing importance in agricultural sciences.

figure 2

Illustration from von Seelhorst ( 1902 ), showing the quite sophisticated outdoor installation “Vegetationskasten” (growing boxes, translations by the author) to weigh plants in small waggons, with a “Kastenwagen” (boxwaggon), b “Waagebalken” (scale beam), c “Deckbretter” (cover board) and d “Waagentisch” (weighing table)

With regard to species differences in water requirement among crops, Schröder ( 1895 , cited in Maximov 1929 ) found two groups, among seven cereals, which differed in water requirement by a factor of 2. Millet, sorghum and maize were known to be drought resistant, and showed a lower water requirement than the remaining plants. These differences were confirmed by Kolkunov ( 1905 , cited in Maximov 1929 ), Briggs and Shantz ( 1914 ), Briggs and Shantz ( 1917 ) and Shantz ( 1927 ). Millet, sorghum and maize are now known to use the C4 carbon pathway of photosynthesis.

With regard to external environmental influences on plants, Briggs and Shantz ( 1913b ) distinguished between soil, atmosphere and plant factors. Soil factors which were investigated were soil moisture content, soil type, cultivation, soil volume, soil temperature, effect of fertilisers in soil or water cultures and effect of previous crops. Weather factors considered were air temperature and humidity, shade and carbon dioxide content. Other factors studied in direct relationship to the plants were parasite attacks, relative leaf area, cutting frequency, defoliation, planting density and the age of plants.

A critique of the term “water requirement” was not long in coming. Dachnowski ( 1914 ) wrote, “It is assumed by many writers that a definite and quantitative relation exists between transpiration and growth, and that hence the ratio of the weight of water absorbed and transpired by a plant during its growth to the green or dry substance produced is an adequate and simple measure of growth.”, followed by an argument why this was not the case.

6 Why do plants differ in transpiration efficiency?

The adaptations of plants to dry environments were an important ecological topic at the beginning of the twentieth century, as the discipline of “physiological ecology” (Iljin 1916 ; Moore 1924 ) began to develop. Iljin ( 1916 ) studied more than 20 different plant species in situ from different ecological locations, e.g. wet bottom soils and variously facing slopes of ravines with different aspects. Iljin proposed that “the water requirements of the different species should be very different, and consequently the amounts of water available should differently affect their processes of life”. Using his observations, he was able to show that “… in no case was the water loss per unit of decomposed CO 2 found to be equal to or more in xerophytes than in mesophytes”, thus suggesting a higher transpiration efficiency. He argued that mesophytes would have to close stomata “… in dry places in order to reduce evaporation, thus diminishing the rate of assimilation as well, whereas in the case of xerophytes, which are adapted to extreme conditions of existence, assimilation in similar circumstances proceeds actively”. He then tried to confirm his hypothesis by transplanting mesophytes from wetter sites to the drier environment of xerophytes. Iljin showed experimentally that in all cases, a higher water requirement was measured for mesophytes transferred to a drier site compared to their original site and compared to xerophytes at the dry site. He interpreted his observations as “plants growing in dry places are adapted to a more economical consumption of water”. He held this to be true for among- and within-species variation.

A milestone in forest “physiological ecology” was Bates’ ( 1923 ) study of the physiological requirements of Rocky Mountain trees. Bates wrote that for foresters, knowledge of demands of tree seedlings for moisture, light, heat and soil fertility was important for planning reforestation. He started a large investigation of six forest tree species, combining field studies to describe ecosystems, with experiments in controlled environments in order to determine species differences in relative transpiration and other water flow-related traits. Bates concluded from the comparison among species that trees of low water requirement would be trees that have a superior control over their water supply. He was however critical of a direct relationship between water requirement and drought resistance in trees. Moore ( 1924 ) commented that in correlating physiological measurements with the habitat characterisation of the species, Bates “... has opened new fields to forest investigations”. He also stressed that the results were counterintuitive in that the most xerophytic species had the highest water requirement, whereas the most mesophytic species had the lowest water requirement.

A similar discrepancy was observed by Maximov ( 1929 ) in the chapter “Efficiency of transpiration” in his book The Plant in relation to water , which was translated from Russian into English rapidly after its publication. Maximov preferred “efficiency of transpiration” to “water requirement”, arguing that the former would be more logically correct, because the determining process (transpiration) should be in the denominator, which also would have the effect that “… an increase in the figure denoting the value of the ratio actually corresponds to an increase of the efficiency per unit of water used”.

In his book, Maximov ( 1929 ) described experiments done at Tiflis Botanic garden (today in Georgia) by Maximov and Alexandrov ( 1917 ), where they studied local xerophytes for 3 years. They found xerophytes with a high efficiency of transpiration, particularly drought-resistant annuals. They also found that plants with a low efficiency of transpiration appeared to be the most typical semi-arid xerophytes. The mesophytes all displayed a medium efficiency. Maximov noted from other observations on the same plants that the “… majority of xerophytes with a low efficiency of water expenditure possess very extensive root systems, far exceeding in length the sub-aerial portions of the plant”. He also observed that these plants showed a strong transpiration and that this transpiration might constitute the “pump” which could draw water through such an extensive root system. He also observed that “members of the group of annual xerophytes with a high efficiency of transpiration are characterised by a relatively large leaf surface, which develops very rapidly”. He argued that this would confer a high intensity of assimilation. From these observations, he concluded a “lack of direct proportionality between efficiency of transpiration and the degree of drought resistance”, but also that “the magnitude of the efficiency of transpiration affords one of the most satisfactory tests of the ecological status of a plant”. Maximov applied the ecological classification developed by Kearney and Shantz ( 1911 ), which they had based on plants of the arid and semi-arid regions of North America: (1) drought-escaping with an annual growth cycle restricted to favourable conditions; (2) drought-evading, delay by various means the exhaustion of soil moisture; (3) drought-enduring, can wilt or dry but remains alive; and (4) drought-resisting, can store a water supply. It should be noted that the ecological definitions behind these concepts have changed with time and are used slightly differently today. Shantz ( 1927 ) argued that many of the drought-evading plants had a low water requirement and Maximov noted that this group included the highly efficient xerophytes with a large leaf area. Maximov also observed that xerophytes from the third group (drought-enduring) could show a very low efficiency of transpiration and belonged to the group of xerophytes with large root systems. Without concluding directly, he suggested a relationship between the transpiration efficiency of a xerophyte and its ecological strategy when facing limited soil water content. These studies by Maximov are among the most complete concerning the relationship between a plants’ resistance to drought and their transpiration efficiency, reflecting the interest of scientists in ecological questions of plant functioning, especially in relation to drought.

Although work on crop plants advanced greatly in the early twentieth century, results were scarcer for tree species. Raber ( 1937 ) concluded his book on “Water utilization by trees, with special reference to the economic forest species of the north temperate zone” with detailed discussions of available data for forest trees. He commented that “much more work on the water requirements of trees of all ages and under varying site conditions is needed”. And he continued that “In view of the importance of planting drought-resistant species in regions where the water supply is below the optimum for most tree species, it is extremely urgent to know more about what qualities make for drought resistance and what species possess these qualities to the greater degree.” These conclusions by Raber show that from the beginning of the twentieth century, the estimation of transpiration efficiency had taken an important place in ecological studies on forest tree species, however not without some critical thoughts on the subject.

7 What is the functional importance of transpiration?

Already in the 1870s and 1880s, the role of stomata in the diffusion of carbon dioxide into the leaf (during the day) and out of the leaf (during the night) was discussed in the scientific literature, as shown by the extensive literature review by Blackman ( 1895 ) (see also section 4 above). Especially the functional importance of transpiration was an open question. There were two opposing lines of thought. As summarised by Iljin ( 1916 ), one defended the line of inquiry that transpiration was important only in the process of transporting mineral salts from roots to leaves; the other held that the opening of stomata was necessary for absorbing the carbonic acid from the atmosphere, which leads to a loss of water and is described as an “inevitable evil”. Iljin ( 1916 ) preferred the second line of investigation and attributed a major role to the stomatal aperture, which controlled both the absorption of carbonic acid from the atmosphere and the loss of water. He concluded that in “physiologico-ecological” investigations, assimilation should be studied together with transpiration. Maskell published a series of papers in 1928, where especially “XVIII.—The relation between stomatal opening and assimilation.” (Maskell and Blackman 1928 ) used an apparatus to estimate apparent CO 2 assimilation and transpiration rate in parallel (Fig. 3 ), and was therefore able to study in detail their interdependence, developing the first mathematical descriptions, based on the development of the theories about the diffusion of gases (Brown and Escombe 1900 ). Methodological advances intensified research on the leaf-level relationship between assimilation and transpiration and allowed the study of plant functioning in more detail. The major step forward was the construction of an infrared gas analyser (URAS: in German “Ultrarotabsorptionsschreiber”, IRGA, infrared gas analyser) by Lehrer and Luft in 1938 (Luft 1943 ) at a laboratory of BASF, IG Farbenindustrie. Normally used in industry and mining, Egle and Ernst ( 1949 ) may have been the first to describe the use of the URAS for plant physiological measurements. By 1959, the URAS was routinely used for measuring stomatal resistance or transpiration in parallel and simultaneously with CO 2 assimilation, on the same leaf (Rüsch 1959 ). This was a great improvement on previous methods and led rapidly to a set of equations for calculating assimilation and stomatal conductance (Gaastra 1959 ).

figure 3

Two figures taken from Maskell and Blackman ( 1928 ): on the top, Figure 1 (p. 489) showing a “Combined assimilation chamber and porometer for simultaneous investigation of apparent assimilation and stomatal behaviour. A. Section of leaf chamber passing through porometer chamber. B. Back view of leaf chamber showing also air-flow meter attached by pressure tubing to porometer and to leaf chamber”. On the bottom, Figure 5 (p. 497) “Relation between porometer rate and apparent assimilation at ‘high’ light, December 1920.” Exp t LI and LII correspond to 2 days of continuous measurements to what Maskell called “diurnal march”

Scarth ( 1927 ) argued that there would be little advantage for a plant to have a high rate of transpiration, but stressed the “... advantage of maintaining the fullest diffusive capacity of the stomata and the highest possible pressure of CO 2 in the intercellular spaces”. He concluded that the principal function of stomata “... is to regulate that very factor which is presumed to regulate them, viz. the concentration of CO 2 in the leaf or, respectively, in the guard cells”. Maskell and Blackman ( 1928 ) tested this hypothesis experimentally and concluded that the rate of uptake of carbon dioxide was determined by variations in stomatal resistance and by resistances within the leaf, thereby introducing the importance of the CO 2 concentrations in the chloroplasts. The suggestion of a strong link between the leaf internal carbon dioxide concentration and leaf-level WUE represented a large advance in the theoretical understanding of WUE.

Penman and Schofield ( 1951 ) proposed, perhaps, the first theoretical link between the leaf-level transpiration ratio (leaf transpiration divided by assimilation) and the ratio of the coefficients of diffusion of water vapour and carbon dioxide in air, and the water vapour and carbon dioxide air-to-leaf pressure gradients. Gaastra ( 1959 ) suggested that the leaf internal conductance to carbon dioxide is a pivotal point of the ratio of assimilation to transpiration and of the water economy of crop plants. Bierhuizen and Slatyer ( 1965 ) showed that the transpiration ratio could be predicted from water vapour and carbon dioxide gradients over a range of light intensities, temperatures and relative humidities. These studies were the first to suggest that whole plant transpiration efficiency might be regulated directly by leaf functioning and would be therefore a trait in its own right and not only the ratio of two plant traits.

8 How can the transpiration ratio be improved?

Because water is increasingly scarce in a warming world, Rüsch ( 1959 ) queried whether the luxury of highly transpiring tree species could be justified. He argued for selective breeding of tree species varieties with low transpiration-to-assimilation ratio T/A by means of minimising transpiration while maximising assimilation. Also Polster et al. ( 1960 ) assessed the potential suitability of tree species to sites by their dry matter production and transpiration ratio. Troughton ( 1969 ) and Cowan and Troughton ( 1971 ) suggested that genetic selection of plant varieties could be used to improve the transpiration ratio by decreasing leaf internal resistance to carbon dioxide diffusion. Cowan and Farquhar ( 1977 ) built on this theme by proposing that stomata might optimise carbon gain to water lost by varying the conductances to diffusion and thereby maximising the ratio of the mean assimilation rate to mean rate of evaporation in a fluctuating environment. Approaches which target photosynthesis, stomatal opening, leaf internal resistance to carbon dioxide diffusion or stomatal optimisation in order to improve plants performance have since been followed in plant breeding and have largely been reviewed elsewhere (e.g. Condon et al. 2004 ; Cregg 2004 ; Vadez et al. 2014 ).

9 Intrinsic water use efficiency and carbon stable isotopes

Another milestone towards contemporary research on water use efficiency was the use of stomatal conductance to water vapour rather than transpiration by Farquhar and Rashke ( 1978 ) and to calculate water use efficiency as assimilation divided by stomatal conductance. This definition allowed an estimation of water use efficiency resulting only from plant functioning, without a direct impact from leaf-to-air vapour pressure difference and was named by Meinzer et al. ( 1991 ) “intrinsic water use efficiency” (W i ). Knowledge of W i facilitated the search for a genetic basis of within species variation, e.g. Brendel et al. ( 2002 ), Condon et al. ( 2002 ) and Chen et al. ( 2011 ).

Development of the stable carbon isotope method for estimating W i resulted in a widely applicable screening method, and a large increase of publications around plant water use efficiency. Based on the two-step fractionation model (atmospheric CO 2 – leaf internal CO 2 – plant carbon) proposed by Park and Epstein ( 1960 ), various models explaining the difference in carbon isotope composition between atmospheric CO 2 and plant carbon were developed in the late 1970s and early 1980s, e.g. Grinsted ( 1977 ), Schmidt and Winkler ( 1979 ) and Vogel ( 1980 ). Vogel’s model contained many theoretical aspects which, however, lacked experimental understanding. In parallel, Farquhar ( 1980 ) developed a similar model, but which resulted in a simple, elegant mathematical equation relating plant natural abundance carbon isotope discrimination, relative to atmosphere, to the ratio of leaf internal to atmospheric CO 2 concentration. This was, in turn, related to W i . Experimental evidence showed that carbon isotope measurements, in wheat, reflected long-term water use efficiency (Farquhar et al. 1982 ) as well as whole plant transpiration efficiency (Farquhar and Richards 1984 ). They concluded that carbon isotope discrimination may provide an effective means to assess and improve WUE of water-limited crops. Strong correlations between whole plant TE and stable carbon isotope measurements of plant organic material were shown in a host of papers to be. Some of these papers were (1) for crops and other annuals (Hubick et al. 1986 ; Ehleringer et al. 1990 ; Virgona et al. 1990 ) and (2) for trees (Zhang and Marshall 1994 ; Picon et al. 1996 ; Roupsard et al. 1998 ). The isotopic method has spread rapidly as a general estimator of WUE and continues to be used widely in screening programmes for plant improvement as well as in ecological research, e.g. Rundel et al. ( 1989 ) and notably used in tree rings (McCarroll and Loader 2004 ).

10 Closing remarks

Water use efficiency is probably one of the oldest of plant traits to stimulate across the centuries the interest of philosophers, theologians, Middle Age savants, natural philosophers and modern plant scientists across different disciplines (plant physiology, ecophysiology, ecology, genetics, agronomy). The interest began as a purely philosophical one, progressed to thought experiments, towards an interest in plant functioning and its relationship to the environment.

Already in the early Renaissance (mid-fifteenth century), an experimentation was proposed, in a time when botany consisted mainly of naming plants (Morton 1981 ). It is then also an early example of an actually performed experimentation, the famous willow experiment by Van Helmont ( 1662 ) as well as of early “in laboratory” experimentation on plants (hydroponics experiments by Woodward 1699 ). The question of what makes plants grow, between water and soil, kept natural philosophers busy up to the end of the eighteenth century, when the assimilation of CO 2 was discovered and the question finally solved.

Early in the nineteenth century, the interest and experimentation turned to the amount of water that plants would need to grow, in the context of a developing research on agricultural practices (Morton 1981 ). Biomass was used to standardise the water losses which allowed comparisons among species (crops as well as trees) and a beginning study of the impact of different environmental variables.

At the end of the nineteenth century, knowledge on the physiological aspects of CO 2 assimilation and the control of transpiration by stomata had sufficiently advanced, so that scientists started to reflect on their inter-dependency. Was transpiration only a physical process or was there a physiological control? Was transpiration regulated by the dry matter production? Or does the stomatal opening determine the rate of CO 2 assimilation?

At the turn of the twentieth century, the study of species differences led to questioning why these differences did exist. As the discipline of “physiological ecology” developed, “water requirement” was inverted into an “efficiency”, reflecting an evolution from standardising transpiration to a trait in its own right. This introduced ecological questions about the adaptation of plants to dry environments and the relation to transpiration efficiency. Counterintuitive results stimulated the discussion and linked differences in WUE to different ecological strategies.

Methodological and theoretical advances in the description of leaf gas exchange in the mid-twentieth century showed the central role of stomata in the control of transpiration and CO 2 assimilation, leading to the idea that stomata might optimise water losses versus carbon gain. The development of carbon stable isotopes as an estimator of leaf-level WUE was an important step not only to further develop these theoretical considerations, but also towards large-scale studies. In parallel, modelling approaches were developed to scale from leaf-level WUE to whole plant TE, e.g. Cernusak et al. ( 2007 ), and to the field or canopy, e.g. Tanner and Sinclair ( 1983 ).

At least from the beginning of the twentieth century onwards, also critical views on the relationship between water requirement and its relation to growth mostly in terms of yield were published (Dachnowski 1914 ). Viets ( 1962 ) asked “Is maximum water use efficiency desirable?”, especially in terms of crop production. Sinclair et al. ( 1984 ) considered different options for improving water use efficiency, however concluding that most of these have important limitations or drawbacks. This discussion is ongoing, as can be seen by the article published by Blum ( 2009 ): “Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress”.

Exploration and application of transpiration efficiency at the whole plant level, and its derivatives at other levels, are still a very active research field across nearly all levels of forest science: concerning very rapid processes at the leaf level (Vialet-Chabrand et al. 2016 ), up-to-date genetic and genomic approaches for breeding (Plomion et al. 2016 ; De La Torre et al. 2019 ; Vivas et al. 2019 ), studying local adaptation of trees to their environment in a population genetic context (Eckert et al. 2015 ) or an ecological context (Pellizzari et al. 2016 ), water use efficiency from the plant to the ecosystem (Medlyn et al. 2017 ), estimated at the population level (Rötzer et al. 2013 ; Dekker et al. 2016 ) or modelling up to the global earth level (Cernusak et al. 2019 ), just to name a few. Thus, the first curiosity of Greek philosophers has motivated scientists through history, with many exciting discoveries still to come.

Change history

17 june 2021.

A Correction to this paper has been published:

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Much of the historical background is based on A.G. Morton’s “History of Botanical Sciences” as well as to Frank N. Egerton’s “A History of the Ecological Sciences” series in the “Bulletin of the Ecological Society of America”. The author is also largely indebted to C. Schuchardt from the Library of the Staatsbetrieb Sachsenforst for help with the quest for rare German publications. The author would also like to thank E. Dreyer and J.M. Guehl (both from the SILVA Unit at INRAE Nancy, France) who commented extensively on an earlier version of the draft and J. Williams (University of Sussex), L. Handley and J. Raven (University of Dundee) who made many valuable suggestions and improved language.

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Brendel, O. The relationship between plant growth and water consumption: a history from the classical four elements to modern stable isotopes. Annals of Forest Science 78 , 47 (2021).

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Article Contents

Introduction, source and sink definitions, source and sink tissues, co-limitation and optimization, sources and sinks affect growth and yield, regulation of sinks and sources, alternative perspectives on growth, conclusions and recommendations, acknowledgements.

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How can we make plants grow faster? A source–sink perspective on growth rate

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Angela C. White, Alistair Rogers, Mark Rees, Colin P. Osborne, How can we make plants grow faster? A source–sink perspective on growth rate, Journal of Experimental Botany , Volume 67, Issue 1, January 2016, Pages 31–45,

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Growth is a major component of fitness in all organisms, an important mediator of competitive interactions in plant communities, and a central determinant of yield in crops. Understanding what limits plant growth is therefore of fundamental importance to plant evolution, ecology, and crop science, but each discipline views the process from a different perspective. This review highlights the importance of source–sink interactions as determinants of growth. The evidence for source- and sink-limitation of growth, and the ways in which regulatory molecular feedback systems act to maintain an appropriate source:sink balance, are first discussed. Evidence clearly shows that future increases in crop productivity depend crucially on a quantitative understanding of the extent to which sources or sinks limit growth, and how this changes during development. To identify bottlenecks limiting growth and yield, a holistic view of growth is required at the whole-plant scale, incorporating mechanistic interactions between physiology, resource allocation, and plant development. Such a holistic perspective on source–sink interactions will allow the development of a more integrated, whole-system level understanding of growth, with benefits across multiple disciplines.

Growth rates of plants vary widely: even in constant environmental conditions, relative growth rate can vary six-fold among species ( Grime and Hunt, 1975 ). This is not surprising given the astonishing variety of ecological niches occupied by plants in all the major biomes, where adaptation comes in part from matching growth rate to available resources ( Díaz et al. , 2004 ). Growth is controlled by proximate physiological and developmental mechanisms, but ultimately depends upon ecological adaptations and evolutionary history: plants with different growth strategies succeed in different ecosystems, and in different niches within those ecosystems. For example, in the dynamic, diverse rainforest environment, rapidly growing seedlings and lianas will quickly colonize gaps, while slow-growing epiphytes often stay poised and wait for a gap in the canopy before upregulating their rates of photosynthesis and growth ( Hubbell and Foster, 1992 ). Ecological life history theory points towards a growth-survival trade-off (e.g. Baraloto et al. , 2010 ), which helps to explain species differences in growth rate ( Metcalf et al. , 2006 ), and leads to niche partitioning ( Wright et al. , 2010 ). Growth rate therefore represents a major axis of ecological variation among species, which correlates with changes in resource availability and risk of mortality, but trades off against defence and storage ( Grime, 1977 ; Herms and Mattson, 1992 ; Rose et al. , 2009 ; Turnbull et al. , 2012 ).

Proximate causes of growth rate variation include both external and internal factors ( Körner, 1991 ). Externally, plants are affected by a plethora of abiotic and biotic factors including nutrient and light levels, temperature, competition, and herbivory, all of which influence the supply and demand for essential resources, and plants must ensure that growth rates are attuned accordingly ( Bloom et al. , 1985 ; Coley et al. , 1985 ). Internally, plant growth is constrained by molecular, physiological, and developmental processes: metabolic rates determine the capacity to take up and store resources, while allocation during development, rates of cell division and expansion, and developmental transitions from vegetative to reproductive growth all have important effects on resource use and partitioning. These internal processes can all be understood within the framework of source–sink interactions: source activity refers to the rate at which essential external resources are acquired by the plant and made available internally, while sink activity refers to the internal drawdown of these resources. This drawdown encompasses resource sequestration in growth and storage, plus resource losses through respiration or exudation. By necessity, the relationships between sinks and sources are both finely tuned and tightly regulated by feedback and feedforward mechanisms, many of which are now well characterized within tissues at the molecular level (e.g. Smith and Stitt, 2007 ; Lawlor and Paul, 2014 ). Since plants are sessile and can only influence external factors to a limited degree, the internal factors are well controlled. As a consequence, it is these internal interactions of source and sink activity that must be responsible for the large intrinsic variation in relative growth rate among species under common environmental conditions.

The general principles governing the diversity in intrinsic growth rate among wild species also underpin the variation in yield potential among crop genotypes. The current need to increase crop productivity for food and fuel, due to a rapidly increasing global population, is urgent and well-documented ( FAO et al. , 2014 ). Yield increases in rice and wheat due to breeding and genetic techniques are currently around 1% per year—a trajectory too low to meet future requirements, and this has motivated the development of global consortia for crop improvement ( von Caemmerer et al. , 2012 ; Reynolds et al. , 2012 ; Ort et al. , 2015 ). The primary focus for many of these is boosting photosynthetic carbon acquisition (source activity), yet sink activity is also believed to limit grain development in many major crops ( Acreche and Slafer, 2009 ; Peterhansel and Offermann, 2012 ; Slewinski, 2012 ). Global efforts to elucidate the responses of crop photosynthesis and yield to future elevated atmospheric CO 2 conditions show that the translation of a large and sustained stimulation of photosynthesis into growth and yield differs markedly between species and often falls short of the expected response ( Long et al. , 2006 a ). Achieving future yield targets requires that this translation of improved photosynthesis into yield is made effectively through enhanced sink development. To achieve the 70% increase in crop productivity required by 2050, a greater understanding of the relationships between photosynthesis and growth, and the factors underpinning growth rates, is therefore essential.

This review discusses current understanding of plant growth rates, considering a range of factors from molecular to ecological, with a particular focus on source–sink interactions. It emphasises the importance of sources and sinks as determinants of growth and as targets for crop improvement. For the first time, this review argues the case for a fully integrated network analysis of physiology, allocation, and development when considering growth across the diversity of wild and crop plants. It highlights source and sink limitation as key areas where understanding could be improved, and suggests that quantitative estimates are required of how sources and sinks limit growth, the extent to which these limitations change at different stages of development within the same species, and their differences in species, which vary in allocation and life history strategies.

Source tissues are net exporters of an elemental resource required for plant growth, such as carbon or nitrogen, while sink tissues are net importers and are responsible for resource assimilation. Mature leaves are net sources of carbon but sinks for nitrogen, while root tissues are net sources of nitrogen but sinks for carbon. Cells require carbon and nitrogen for growth and development; nitrogen to maintain protein turnover; and carbon for respiration to fuel metabolic processes. Other elements are also vital for growth, such as oxygen obtained from the air, hydrogen from water, and minerals found in soil including the macronutrients potassium and phosphorus, and numerous micronutrients. This review focuses on carbon and nitrogen only, because these elements are commonly limiting for growth, and effectively illustrate the balance between source and sink tissues. Carbon is usually exchanged between sources and sinks as simple sugars, typically sucrose. The equivalent currency of exchange for nitrogen includes both inorganic ions (NO 3 – ) and organic forms (typically amino acids).

Source tissues are generally responsible for the acquisition of resources from the external environment, although the remobilization of stored resources (e.g. to subsidize reproduction or regrowth after disturbance) may also turn a sink into an internal source. A general definition of source strength should therefore consider the export rate of a particular resource from the source tissue. However, C- or N-uptake from the external environment is more commonly and easily measured than internal fluxes of sucrose or inorganic and organic nitrogen. Consequently, the term ‘source strength’ usually refers to the net rate of uptake (mol s –1 ) for a particular resource from the external environment:

where source size refers to the total biomass of source tissue (g), and source activity is the specific uptake rate of the resource (mol g –1 s –1 ; based on Geiger and Shieh, 1993 ).

Sink tissues are net receivers of resources from source tissues ( Doehlert, 1993 ). While all tissues have some sink activity, leaves are net sinks for nitrogen transported from the root system, and roots are net sinks for sucrose exported from leaves. Sink strength refers to the net rate of uptake (mol s –1 ) for a particular resource by a defined tissue within the plant:

where sink size is the total biomass of sink tissue (g), and sink activity refers to the specific uptake rate of the resource (mol g –1 s –1 ). Sink activity involves the utilization of resources for the synthesis of new tissues, including the synthesis of structural components such as cell walls, or the maintenance and modification of existing tissues, including the synthesis of non-structural components including enzymes, storage and defence compounds. Sink activity also encompasses the expenditure of resources in respiration or root exudation. In practice, therefore, it is usually quantified via the net accumulation rate of a particular resource in a tissue over time, after accounting for the losses from respiration and exudation.

Source tissues thus take up resources from the environment and export them to sinks, which draw down resources within the plant. The parallels with financial transactions are clear in this conceptualization of plant function, and the next section considers the molecular currencies traded between sources and sinks.

Mature leaves are net sources of carbon. Carbon dioxide is fixed to generate triose phosphate in photosynthesis, which is then converted to starch for diurnal storage in the chloroplast ( Smith and Stitt, 2007 ; Gibon et al. , 2009 ; Stitt and Zeeman, 2012 ; Pilkington et al. , 2015 ), or to sucrose for export from the leaf or storage in the vacuole.

Net carbon sink tissues include roots, tubers, reproductive structures, and young leaves. Sucrose may itself be stored directly, or it may first be converted to storage polymers. These polymers are typically starch or fructans, depending on the species; some plants store additional compounds such as raffinoses ( Atkinson et al. , 2012 ). Starch is stored in the amyloplasts and chloroplasts of many higher plants ( Müller-Röber et al. , 1992 ); amyloplasts are found in seeds, shoot storage tissues, and roots, while chloroplasts are found in leaves and stems (and are the only repository for starch within leaves). Starch is also the primary carbohydrate in the grains of many crops, including wheat, rice, and maize, and in the tubers and storage roots of vegetables ( Pollock and Cairns, 1991 ; Zeeman et al. , 2010 ). Carbon storage in the stems of many temperate grasses consists primarily of fructans ( Pollock and Cairns, 1991 ; Scofield et al. , 2009 ), water-soluble fructose polymers which confer some resistance to low temperatures ( Sandve et al. , 2011 ). Typically, fructans and sucrose are stored together in the stem, as in wheat, barley, and oat ( Slewinski, 2012 ). Significant stem storage of starch is rare in cereals—rice being a notable exception, storing sucrose in leaves and starch in stems ( Murchie et al. 2009 ), and being unable to synthesize fructans naturally ( Kawakami et al. , 2008 ). Stem storage of carbohydrates is an important buffering system for recovery after grazing and for supplying photosynthate to cereal ears during grain-filling, especially during drought ( Schnyder, 1993 ; Ruuska et al. , 2006 ; Slewinski, 2012 ), and is thus a relatively labile sink. For growth, a major use of photosynthate is the synthesis of cell wall polysaccharides such as cellulose and hemicellulose, in all parts of the plant. Indeed, almost half of plant cell wall biomass is composed of carbon ( Körner, 2012 ).

In addition to the assimilation of resources in sink tissues, the utilization of resources in respiration and exudation constitute a further sink, since these processes also contribute to resource drawdown. Maintenance respiration can represent a significant carbon cost to the plant ( Penning de Vries, 1975 ); for example, respiration constitutes 70% of the carbon sink in Pinus halepensis ( Klein and Hoch, 2015 ). Carbon and nitrogen are released through root exudation of a variety of compounds including organic acids, sugars, polysaccharides, ectoenzymes such as acid phosphatase, and sloughed-off cells and tissues ( Marschner, 1995 ). Exuded metabolites have many functions ( Badri and Vivanco, 2009 ) such as modifying the rhizosphere to provide a desirable environment for beneficial microorganisms and providing signals to aid recruitment of arbuscular mycorrhizal fungi, contributing to immunity ( Cameron et al. , 2013 ). These processes may be substantial—one meta-analysis of annuals found that 30–60% of net photosynthetic carbon is allocated to roots, of which 40–90% is lost in respiration and exudation ( Lynch and Whipps, 1990 ).

In contrast to carbon, roots are net sources for nitrogen, while shoot tissues are net nitrogen sinks until senescence when their nitrogen is remobilized ( Aerts and Chapin, 2000 ). Annuals remobilize nitrogen for reproduction while perennials may remobilize nitrogen for reproduction or for growth and storage in subsequent years. Inorganic nitrogen is taken up by roots as nitrate (NO 3 – ) or ammonium (NH 4 + ), and may be utilized in growth or exported from the root. Assimilation of nitrogen into amino acids takes place in both roots and shoots, although the relative proportions depend on the species and are still debated ( Nunes-Nesi et al. , 2010 ). Approximately 80% of wild plant species benefit from mycorrhizal associations in which specialised fungi aid the uptake of phosphorus and sometimes organic nitrogen ( Read, 1991 ). Organic nitrogen may also be taken up from the soil in the form of free amino acids. Nitrogen is exported from roots as nitrate (transported in the xylem), amino acids or amides (both transported in the phloem).

Root and leaf nitrogen concentrations are positively correlated, but a global survey of wild grassland species found that leaf nitrogen concentration is more than double that of roots in the same species ( Craine et al. , 2005 ). The main use of nitrogen for growth is in proteins and there is a particularly high demand in leaves, where the complex, enzyme-rich photosynthetic machinery is assembled and maintained. Photosynthetic proteins encompass the majority of leaf nitrogen—for example, Rubisco (EC typically accounts for between 10% and 30% of leaf nitrogen content but can account for up to 50% of leaf nitrogen content ( Ellis, 1979 ; Sage et al. , 1987 ; Evans, 1989 ). Through Rubisco, carbon source activity is directly connected with leaf nitrogen sink activity, providing one way in which source and sink activity are intrinsically coordinated. Nitrogen partitioning into photosynthetic proteins is a flexible trait, varying between species and as resource availability changes ( Evans, 1989 ).

Nitrogen may be stored as nitrate in the vacuole, or as proteins ( Millard, 1988 ). Vegetative storage proteins (VSPs) may comprise up to 50% of soluble protein in vegetative tissues ( Liu et al. , 2005 ). Protein storage occurs primarily in seeds, although some legumes, tuber-formers, and deciduous trees species have additional storage proteins ( Shewry, 1995 ). VSPs have been well-studied in soybean, and the nitrogen sink-to-source transition occurring in leaves during ontogeny is correlated with a decrease in VSP gene expression in this species (reviewed by Staswick, 1990 ). In both potato and soybean, removal of nitrogen sink tissues upregulates nitrogen storage in other parts of the plant, indicating a buffering role for VSPs in maintaining source:sink balance ( Staswick, 1990 ). In contrast, grasses such as wheat and rice (usually grown as annuals) are less reliant on protein stores beyond those in the seed, yet can still accumulate nitrogen when conditions are favourable. For example, excess nitrogen in wheat accumulates in the lamina of upper leaves or the true stem of the peduncle, and just as stem carbohydrate reserves are important for grain-filling in grasses, this stored nitrogen is thought to provide a nitrogen buffer for use during grain-filling ( Pask et al. , 2012 ). Non-leaf nitrogen stores, such as the culm in grasses, may also play a role in plant recovery after grazing.

A plant that has optimized its source:sink ratio can grow using balanced allocation of source and sink sizes and activities (Equations 1–2), facilitated by molecular feedbacks. However, at any point in time, most plants are not fully optimized, meaning that the creation of either more source or sink tissue could increase growth: in these cases, the potential source or sink strength (Equations 1–2) has not been realized ( Patrick, 1993 ). The extent to which these potentials are met may be investigated using environmental or genetic manipulations, and are discussed later in this review.

Resource uptake changes over time due to fluctuations in the external environment, such that the total supply of a particular resource over the lifetime of the plant cannot be predicted in advance. The plant reacts to these fluctuations in resource availability by modifying its investment in resource acquisition and consumption ( Freschet et al. , 2015 ). At the most general level, a suitable balance between leaf and root tissues is critical for balancing the acquisition of carbon and mineral nutrients. Allocation to shoot and root is adjusted depending on available resources so that, for example, the allocation of resources to root growth is increased in low nitrogen soil conditions. Co-limitation by carbon and nitrogen has been demonstrated experimentally and optimization of these resources has been considered in models ( Woodrow, 1994 ; Iwasa, 2000 ; Guilbaud et al. , 2015 ) yet, due to environmental and developmental constraints, plants do not always achieve perfect co-limitation in vivo .

Greater insights into this balancing of sources and sinks at the whole-plant scale can be gained by analogy with metabolic systems within cells or tissues. In plant metabolic networks, control of the overall flux is typically shared between several enzyme steps, although many elements in the system exert only a limited effect ( Fell and Thomas, 1995 ; e.g. Raines, 2003 ; Araújo et al. , 2012 ). If the dynamic internal system of resource fluxes among source and sink tissues is analogous to such a metabolic system, then overall control of the flux of materials into growth is also likely to be shared among multiple elements. This flux control analogy generates two predictions.

The first prediction is that multiple elements in the system share control of the growth rate, and growth will increase if their sizes or activities are raised together. In contrast, most elements exert limited control, and are present in excess. The most resource-efficient solution for the developing plant is therefore to tune down investment in those components with little influence, and increase allocation to the elements exerting a high degree of control. Such regulation must be a dynamic process that balances fluctuations in external resource availability with ontogenic changes in the demand for resources. Analogous examples from metabolism show how such reallocation among elements in the system can optimize enzyme activities to increase fluxes ( Woodrow, 1994 ; Zhu et al. , 2007 ). However, in a whole-plant system, this optimization process must operate within the context of life history strategies of investment in growth versus defence or storage (the growth–survival trade-off).

The second prediction generated by the flux control analogy is that development of new source and sink organs during ontogeny shifts the overall control of growth to different elements in the system. This effect is expected because changes in the number, size, and activity of plant organs during development alters the internal capacity of a plant to acquire and consume resources, and is well supported by experimental evidence. For example, some plants transition from sink to source limitation during the shift from vegetative to reproductive growth (examples within Arp, 1991 ; Marschner, 1995 ; Rogers and Ainsworth, 2006 ). Equivalent effects arise when plants are exposed to external environmental conditions which change resource acquisition rates, or if the numbers or activities of source or sink organs are manipulated experimentally. The evidence for such effects is considered in the next section of this review.

In combination, these external and internal factors mean that the acquisition and consumption of resources must be balanced over time by a combination of coarse and fine internal regulatory controls. This control, in turn, operates within a general life history strategy of investment in growth versus storage or defence, which means that the growth rate is not necessarily maximized under particular internal and external constraints.

The situation for crop plants is simpler, since breeders aim to maximize lifetime growth and reproductive allocation within monospecific communities ( Denison, 2012 ). Current views on source–sink relations in crop plants point towards a co-limitation of growth by sources and sinks during grain-filling ( Álvaro et al. , 2008 ; Acreche and Slafer, 2009 ; Peterhansel and Offermann, 2012 ; Slewinski, 2012 ) yet growth could be further optimized. One line of evidence for the lack of optimization of source and sink to maximize growth comes from experiments where plants are grown at elevated CO 2 (discussed later, in Table 1 ). Such experiments aim to predict the responses of plants to future climatic conditions, and increase the carbon source activity of plants in a non-invasive manner. The increase in photosynthesis under elevated CO 2 demonstrates that source activity typically limits growth under ambient CO 2 levels. However, the increases in photosynthesis and yield seen when plants are grown under elevated CO 2 do not match the magnitude of those predicted from theoretical modelling and extrapolation of chamber experiments ( Long et al. , 2006 a ; Ainsworth et al. , 2008 ; Leakey et al. , 2009 ). These results suggest a degree of sink limitation of growth, which could be due to nitrogen limitation. Responses to CO 2 do vary between species ( Poorter, 1993 ) and some plants are able to upregulate source and sink in concert. For example, high CO 2 can stimulate nitrate uptake to balance source and sink capacity ( Stitt and Krapp, 1999 ). When external nitrate levels are low, elevated CO 2 levels cause an increase in both the rate of nitrate uptake and the activity of a high affinity nitrate transport system in wheat roots ( Lekshmy et al. , 2009 ), representing an upregulation of nitrogen source strength through increased activity [Equation (1)].

Experimental manipulations of the carbon source:sink balance, illustrating that:

(a) both sources and sinks affect plant growth; (b) sources and sinks regulate each other by feedback mechanisms; (c) source and sink strength can be altered by the plant, to alleviate perturbations of the source:sink balance

‘+’ denotes treatments applied in combination; ‘/’ denotes alternative treatments.

In order to improve crop yields, a greater, more integrated understanding of how plant growth rates are limited by sinks and sources for carbon and nitrogen, and the shifts in limitation that occur during the lifetime of a plant, is required. Only by grounding modelling and experimental work in mechanistic knowledge of source:sink relationships will plant growth be effectively understood—and potentially manipulated—at every stage of development in order to maximize yield.

Evidence that growth may be controlled by both source and sink strengths comes from manipulation experiments and studies of natural variation among species.

Manipulation experiments

Manipulating the source:sink balance shows that source and sink strengths often operate below their full potential, due to the limitations imposed by environmental and developmental changes discussed above. Historically, such manipulations involved physically manipulating the plant or its environment: for example, source activity may be altered by elevated CO 2 , defoliation, or shading, while sink activity may be altered by sink removal or sink chilling. However, modern genetic approaches may now be used to alter source and sink activity with greater elegance. Table 1 outlines a range of source:sink manipulations and summarizes their results. Broadly speaking, increasing either source or sink may increase growth, suggesting that both can limit growth to a certain extent. Sources and sinks regulate each other by molecular feedback mechanisms (discussed later), and evidence for these is seen at the whole-plant scale when manipulation of the source affects sink activity, and vice versa .

Elevated CO 2 increases the potential carbon source activity of the plant by stimulating photosynthesis, and this typically translates into faster growth ( Table 1 ; e.g. McConnaughay et al. , 1993 ; Christ and Körner, 1995 ; Masle, 2000 ; see also Taylor et al. , 1994 ; Ranasinghe and Taylor, 1996 ; Long et al. , 2006 b ; Ainsworth and Rogers, 2007 ; Leakey et al. , 2009 ), also affecting cell patterning, cell expansion, and plant architecture ( Kinsman et al. , 1997 ; Pritchard et al. , 1999 ; Masle, 2000 ). Growing plants in large pots increases the potential carbon sink activity, due in part to increased nitrogen availability, generally leading to increased growth ( Table 1 ; McConnaughay et al. , 1993 ; Poorter et al. , 2012 ), and experiments comparing species or cultivars with different sink sizes reveal that growth is faster when sinks are larger ( Table 1 ; Reekie et al. , 1998 ; Aranjuelo et al. , 2013 ).

Reduction of source leaf area by defoliation usually leads to an increase in photosynthesis in the remaining leaves, to maintain source activity within the plant and support the sinks ( Table 1 ; von Caemmerer and Farquhar, 1984 ; Eyles et al. , 2013 ). This could indicate sink limitation of growth because leaves are not carrying out their maximal potential rates of photosynthesis under normal conditions. In contrast, decreasing sink capacity—for example, by inhibiting sucrose export from leaves to reduce the apparent sink demand—leads to an inhibition of photosynthesis ( Table 1 ; Ainsworth and Bush, 2011 ) mediated by an increase in leaf carbohydrates ( Sheen, 1990 ).

Combining experimental treatments that affect both source and sink provides evidence that sources and sinks work together and feed back on each other. Photosynthetic acclimation at elevated CO 2 concentration is a decrease in photosynthetic capacity that reduces the magnitude of the CO 2 -induced stimulation in photosynthetic rate at elevated CO 2 . Acclimation acts to reduce the ratio of source:sink activity and thus adjust source:sink balance towards equilibrium. Combining defoliation and elevated CO 2 treatments (which decrease and increase the source, respectively) shows that photosynthetic acclimation under elevated CO 2 is alleviated by defoliation, supporting the hypothesis that it is sink-mediated ( Table 1 ; e.g. Bryant et al. , 1998 ; Rogers et al. , 1998 ; Ainsworth et al. , 2003 ). The alleviation of acclimation occurs because defoliation opposes the effect of elevated CO 2 by decreasing the source:sink ratio, and higher levels of photosynthesis can thus be maintained in the remaining leaves. The opposite effect is seen when the source is increased but the sink is reduced. For example, when physical removal / restriction of sinks or genetic manipulation to reduce sink size is combined with elevated CO 2 , leading to an increase in the source:sink balance, source activity is decreased in order to return towards equilibrium ( Table 1 ; Arp, 1991 ; Ainsworth et al. , 2004 ). Combining low nitrogen or low temperature—which restrict sink development—with elevated CO 2 has a similar effect ( Table 1 ; Arp, 1991 ). In contrast, increasing carbon sink capacity under elevated CO 2 , by using high-yielding cultivars or adding nitrogen, facilitates increased photosynthesis ( Table 1 ; Farage et al. , 1998 ; Aranjuelo et al. , 2013 ).

Differences among species

In some species, developmental plasticity allows for greater flexibility when the source:sink balance is perturbed. Potato and citrus may easily increase their sink size, so tend to suffer less from feedback inhibition of photosynthesis ( Paul and Foyer, 2001 ), and nitrogen-fixing legumes are easily able to increase their sink size in response to elevated CO 2 ( Rogers et al. , 2009 ).

The physical mechanism of carbon export is important for the coordination of source and sink. Growth determinacy in soybean prevents an increase in photosynthesis at high CO 2 , while poplar trees have high photosynthate export and maintain elevated photosynthesis at high CO 2 ( Table 1 ; Ainsworth et al. , 2004 ; Ainsworth and Bush, 2011 ). Species which are symplastic loaders (many trees and shrubs) transport sucrose from source tissues into the phloem through developmentally fixed plasmodesmata, whereas apoplastic loaders (many herbaceous species) use developmentally plastic membrane transporters ( Ainsworth and Bush, 2011 ). Therefore, at high CO 2 , symplastic loaders cannot upregulate photosynthate export to the same extent as apoplastic loaders. As a result they tend to accumulate more non-structural carbohydrates in their leaves ( Körner et al. , 1995 ) and can show a smaller increase in photosynthesis under elevated CO 2 . However, despite their symplastic loading strategy, trees are generally well able to maintain photosynthetic stimulation under elevated CO 2 ( Ainsworth and Rogers, 2007 ) although some species are capable of both symplastic and apoplastic loading and many species have not yet been characterized.

Taken together, this evidence clearly demonstrates that sources and sinks can both limit growth, and that feedbacks enable a degree of compensation. Species with greater plasticity can be more flexible in their response to manipulations of source and sink.

Regulation of source:sink balance is essential for enabling plants to maintain a growth rate appropriate for a given availability of resources. Storage allows the assimilation of more resources than are needed in growth, to create a reserve for future development in a fluctuating environment or recovery from disturbances such as herbivory. However, carbon assimilation must be appropriate for the available sink strength, in order to create a sufficiently large store that is still within the limits imposed by sink potential—thus sinks must feed back on sources to regulate their activity. Similarly, source activity must influence sink strength so that appropriate sinks may develop and plants can fully realize their growth potential for a given resource availability. Furthermore, the high metabolic costs of carbon and nitrogen assimilation mean that regulation of source and sink is vital to avoid wasting energy.

A complex molecular network including carbon- and nitrogen-derived signals and phytohormones has evolved to integrate the uptake, assimilation, and allocation of resources ( Nunes-Nesi et al. , 2010 ). Many mechanisms of these molecular interactions are now well established although the puzzle remains incomplete at the whole-plant scale. Figure 1 illustrates key feedforward and feedback mechanisms regulating the source:sink relationship. Carbon- and nitrogen-derived feedforward and feedback signals act on sources and sinks of both carbon and nitrogen. This allows sources and sinks to modify their own activity, and also to regulate that of other tissues, creating molecular signalling links between source and sink.

A range of feedback mechanisms fine-tunes the source:sink balance and therefore plant growth. Signals derived from both carbon (green) and nitrogen (blue) regulate source–sink relationships. Feedbacks operate at the tissue level (arrows 1–4 and 6–9) and at the whole-plant level (arrows 5 and 10). Narrow grey arrows represent net movement of carbon and nitrogen from source (lighter) to sink (darker) tissues within the plant.

A range of feedback mechanisms fine-tunes the source:sink balance and therefore plant growth. Signals derived from both carbon (green) and nitrogen (blue) regulate source–sink relationships. Feedbacks operate at the tissue level (arrows 1–4 and 6–9) and at the whole-plant level (arrows 5 and 10). Narrow grey arrows represent net movement of carbon and nitrogen from source (lighter) to sink (darker) tissues within the plant.

Carbon feedbacks

Leaf carbohydrates feed into a complex network, affecting transcription, translation, and post-translational processes in order to balance carbon supply and demand (reviewed in Fig. 1 ). For example, a high carbon status upregulates nitrogen source and sink activity ( Fig. 1 ; arrows 7 and 9) and carbon sink activity (arrows 5a and 5c), while downregulating photosynthesis (arrows 2 and 3). In contrast, a low carbohydrate content in the leaf leads to the repression of carbon sink activity (arrow 5b). The presence of such a regulatory feedback loop in the leaf has long been investigated: in 1868, Boussingault first proposed that assimilate accumulation could decrease photosynthesis by feedback ( Neales and Incoll, 1968 ), yet the precise mechanism for sucrose signalling remains unknown ( Reda, 2015 ).

The partitioning of carbon into starch and sucrose is an important point of carbon source–sink regulation (directly affecting arrows 2 and 5 in Fig. 1 ) and is controlled by several factors. For example, trehalose-6-phospate is believed to influence starch synthesis by redox-regulation of AGPase, a key enzyme in starch synthesis, while the degradation of starch is regulated by a variety of enzymes, by the circadian clock, and possibly by starch-derived signals or even the level of starch itself ( Smith and Stitt, 2007 ). It is important to note that most research into sugar and starch regulation has been carried out in Arabidopsis and it is therefore necessary to expand current knowledge of regulatory mechanisms in crop plants, which may not share the same mechanisms. For example, the starch degradation pathway in the endosperm of cereal grains differs from that in Arabidopsis leaves ( Smith, 2012 ), while mutation of PGM, an enzyme important in starch synthesis and essential for normal growth in Arabidopsis , does not affect all species equally, suggesting the use of different metabolic pathways or storage compounds ( Stitt and Zeeman, 2012 ).

Nitrogen feedbacks

Just as carbon availability impacts both on carbon and nitrogen source and sink activities, nitrogen availability regulates the uptake and storage of carbon (reviewed in Fig. 1 ). A high nitrogen status increases the rate of carbon acquisition in photosynthesis and also upregulates carbon sinks ( Fig. 1 ; arrows 1 and 4). Nitrogen also increases the assimilation of nitrate by the enzyme nitrate reductase, to upregulate nitrogen source and sink activity ( Fig. 1 ; arrows 6 and 8), and increases shoot:root allocation, enabling the plant to acquire more carbon and make use of the available nitrogen (arrow 10). Furthermore, nitrate increases root cytokinin production and export ( Fig. 1 , arrow 10), important for meristem generation and function in shoot and root ( Su et al. , 2011 ).

Tight control of the source–sink relationship is facilitated by points of crosstalk between carbon- and nitrogen-signalling pathways. This enables plants to maintain a degree of co-limitation for sources and sinks, and carbon and nitrogen. Starch synthesis is regulated by nitrate as well as by sugar: nitrate downregulates transcription of the gene encoding the regulatory subunit of AGPase, an enzyme involved in starch synthesis. This negative regulation by nitrate lowers starch accumulation and allows more leaf sugar to be exported for growth when nitrate levels are high (discussed by Stitt and Krapp, 1999 ). Leaf sugars are involved in the transcription and post-translational regulation of nitrate reductase ( Fig. 1 , arrow 9), enabling plants to coordinate carbon and nitrogen supply ( Stitt and Krapp, 1999 ; Kaiser et al. , 2002 ): sugars increase the level of nitrate reductase ( Reda, 2015 ) while low sugar levels repress its transcription ( Klein et al. , 2000 ).

Coordination is enhanced still further by crosstalk between sugars and phytohormones [for recent review, see Lastdrager et al. (2014) ]. This contributes to developmental processes such as meristem activity (which is generally upregulated by cytokinins, e.g. Fig. 1 , arrow 4) and lends an added layer of complexity to growth regulation ( Eveland and Jackson, 2012 ). For example, sugars interact with abscisic acid ( Teng et al. , 2008 ) and with auxin ( Stokes et al. , 2013 ). Sugars can also act directly on development, independently of phytohormones, and are believed to be important for regulating meristem activities ( Eveland and Jackson, 2012 ). Furthermore, sugar levels influence the transcription of thousands of genes; sugars and the circadian clock regulate each other; and sugars induce phytochrome-interacting factors, which regulate growth ( Lastdrager et al. , 2014 ).

In summary, molecular feedbacks including carbon- and nitrogen-derived signals regulate sources and sinks for carbon and nitrogen. Crosstalk exists both between these signals and with growth regulators. With such elaborate molecular mechanisms in place—and given sufficient resources—increasing the sink activity of a plant might be expected to increase its source activity, and vice versa. However, as discussed above, experimental manipulations of sink strength and of source strength reveal that growth cannot always be altered as expected (e.g. Long et al. , 2006 a ). It has thus become important to increase knowledge of the potential strengths of source and sink, the limits to their physiological interactions, and to better incorporate known molecular mechanisms of the source–sink relationship into models of whole-plant growth. Moreover, in order to effectively increase crop yield, it may be necessary to manipulate the molecular feedback mechanisms between source and sink, in addition to manipulating the strengths of source and sink themselves. A source–sink-based perspective on growth is therefore an essential cross-disciplinary tool for understanding and increasing the growth and yield of crops.

Different disciplines have alternative perspectives of plant growth. Advancing the mechanistic understanding of growth that is necessary to realize improvements in crop growth will require a unification of these disciplinary perspectives. Here, a parsimonious model of plant growth which unites these different perspectives is presented. An extremely simplified system is used for illustration. Various factors have been omitted for simplicity, clarity, and ease of unification. These are both intrinsic (additional resources and tissue types within the plant, and feedbacks between internal processes) and extrinsic (environmental limitations on physiological and developmental processes), since plant growth and development are the product of genetic and environmental processes (e.g. Prusinkiewicz et al. , 2009 ; Pantin et al. , 2012 ). Rather than provide comprehensive models of growth, this section highlights key processes of interest for each of the three perspectives on growth, and uses equations to demonstrate the focus of each. In each perspective, the processes of interest depend on source and sink activities and tissues, and the equations are finally united to form a basic holistic model of plant growth which is underpinned at every level by source–sink interactions.

Growth may be conceptualized in a number of different ways, and may be viewed through different lenses depending on the perspective adopted. Three classic perspectives on growth are based on: the physiology of resource acquisition and loss; the internal allocation of resources to source and sink organs; and the morphogenetic development of source and sink tissues. Crucially, these three alternative perspectives, adopted by communities of scientists from different disciplines are all readily conceptualized within the context of source–sink interactions.

Here, equations have been used to illustrate each definition of growth, by considering a highly simplified system in which a single resource (carbon) is acquired by a source tissue (leaves) and used by sinks (in both leaves and roots). This system enables the limitations on growth to be formally defined in a readily interpreted form, yet still allows growth to be viewed through the three alternative lenses presented. Each of the three perspectives presented is, by mathematical definition, true. However, each is based implicitly upon an alternative hypothesis about the critical intrinsic controls on growth.

At its most fundamental level, growth may be defined as an increase in plant mass over time. For simplicity, growth is considered equivalent to net organic carbon gain, and the acquisition of other resources is ignored. The dry weight of organic carbon in the plant is W P , referred to in this section as mass, and absolute growth rate (AGR) is thus net carbon gain over time, in g d –1 :

Growth may now be defined in various ways according to the perspective adopted, but the central definition [Equation (3)] is retained. The different approaches to explaining growth focus attention on different primary limitations.

The first approach is physiological: a flux balance of organic carbon for the plant based on the loss and acquisition of this essential resource to and from the atmosphere via the processes of respiration and photosynthesis ( Lambers et al. , 1989 ; Poorter and van der Werf, 1998 ).

This carbon-based balance viewpoint on growth is adopted widely in crop production models and in Ecosystem and Earth System Models (EESMs), which simulate the physical properties and carbon exchange of the vegetated land surface (e.g. Knorr, 2000 ; Sitch et al. , 2003 ; Lu and Ji, 2006 ; Zaehle and Friend, 2010 ), and are ultimately used to project future global change ( Friedlingstein et al. , 2014 ; IPCC, 2014 ). This flux balance approach expresses the AGR as the difference between photosynthesis and respiration:

where A is gross photosynthetic carbon uptake in g C d –1 g -1 leaf mass, W L is total leaf mass (g), and R is respiratory carbon loss in g C d –1 g –1 plant mass. Note that not all of the inorganic carbon captured by photosynthesis is converted to biomass, and so R includes the metabolic costs of biosynthesis, translocation, exudation, and the uptake and assimilation of nitrogen needed for growth (‘growth respiration’), as well as those associated with maintaining existing tissues (‘maintenance respiration’) (reviewed by Amthor, 2000 ).

Respiration may be partitioned between photosynthetic and non-photosynthetic tissues:

where the subscripts L and R denote leaf and root tissues, respectively. A simple case is considered here, but this approach may be easily extended to include other sink tissues such as storage organs, stems, and reproductive tissues.

This basic model views growth as the net accumulation of organic carbon. However, the approach is limited because, while respiration is one component of sink activity, the sink activities of growth and storage are not explicitly considered, and accounting for sink limitation requires modifications to the model ( Fatichi et al. , 2013 ). Furthermore, recent authors have argued that A and R do not control plant growth rate. Instead, it is argued that growth is controlled by the supply of mineral nutrients and water, and the plant regulates A and R to meet its growth requirements ( Körner, 2012 ; Fatichi et al. , 2013 ; Körner, 2013 ). Without accounting for sink activities and their feedbacks on photosynthesis, the approach illustrated by Equations (4a) and (4b) cannot provide a complete description of the processes controlling growth.

A second approach considers the internal allocation of resources to either photosynthetic or non-photosynthetic tissues. These tissues represent net carbon sources and sinks, respectively.

The philosophy underlying this approach is that allocation of resources to leaves (especially to leaf area) accelerates growth, whereas allocation to non-photosynthetic tissues (in this case, roots) has an opposing effect. Allocation is an important determinant of growth rate, and this viewpoint is classically adopted by ecologists when considering the ecological strategies of plants ( Grime and Hunt, 1975 ), resource limitations on growth ( McConnaughay and Coleman, 1999 ; Yang and Midmore, 2005 ), and the growth-allocation trade-off as a constraint on life history decisions ( Bazzaz et al. , 1987 ). It is also considered dynamically in relation to resource limitation in global vegetation models (e.g. Higgins and Scheiter, 2012 ) and in crop simulation models (e.g. Weir et al. , 1984 ; Brisson et al. , 1998 ; Jamieson et al. , 1998 ).

The change in plant mass over time is the product of leaf area ratio, net assimilation rate, and plant mass:

where LAR is leaf area ratio (m 2 leaf area g –1 plant mass) and NAR is net assimilation rate (g carbon m –2 leaf area d –1 ), remembering that carbon is equivalent to mass in these examples.

Viewed through the lens of carbon allocation, growth depends critically on the availability of photosynthetic tissue, expressed as the LAR . The LAR is in turn a product of SLA , the ratio of leaf area to leaf mass (efficiency of leaf area deployment, m 2 g –1 leaf mass), and LMR , the ratio of W L to W P (dimensionless):

Both SLA and LMR vary with W P . At any point in time, by definition, leaf area ( L , in m 2 ) is therefore given by the following equation:

where SLA(W P ) and LMR(W P ) denote W P -dependent values of SLA and LMR . The LAR changes over time in accordance with changes in allocation during growth, and the components of LAR therefore vary with plant mass, W P :

where ∂ S L A / ∂ W P and ∂ L M R / ∂ W P describe the effects of allocation changing over time as plant mass changes.

The allocation perspective on growth, like the physiological perspective, can be interpreted in terms of source–sink interactions. For carbon, leaves constitute a net source while roots constitute a net sink. Thus Equation (5d) describes the change in the carbon source over time, and equivalent equations for roots would describe the change in the carbon sink.

These first two perspectives, which look at growth through the lenses of physiology and allocation, are ultimately resource-driven. The physiological perspective defines growth as being driven by carbon acquisition from, and losses to, the external environment, although in reality sink feedbacks are also important here. The allocation perspective is driven by the allocation of carbon to structures that are responsible for its net acquisition or consumption.


The third perspective encompasses the developmental processes of organ initiation, growth, and termination. These processes represent carbon sinks.

In contrast to the first two approaches, which are resource-driven, the third perspective considers the developmental process explicitly, and this is the approach applied by developmental biologists working on growth in Arabidopsis and crop plants. This perspective also impinges on large-scale macroevolutionary comparisons among species, since the evolution of development must inevitably drive changes in potential growth rate, for example, in transitions between woody and herbaceous life forms ( Dodd et al. , 1999 ) or in transitions between determinate and indeterminate growth ( Shishkova et al. , 2008 ).

Cells divide and expand at a rate that is ultimately limited not by the speed of resource acquisition from the external environment (although this does influence meristem activity, e.g. Pritchard et al. , 1999 ; Granier et al. , 2007 ) but by intrinsic constraints set by the internal resource balance, the cell cycle and developmental programme. Again, internal source–sink interactions underpin these processes. Because cell division and expansion, and the creation of new meristems through branching constitute sinks for carbon, modelling growth from a developmental perspective places greater emphasis on the limitation of growth by sink rather than source activity. Ultimately, cell division rate is limited by molecular constraints: for example, plant genome size is negatively correlated with cell cycle time ( Francis et al. , 2008 ) and with root meristem growth rate ( Gruner et al. , 2010 ).

Complex formulations for organ initiation, expansion, and termination have been developed, but a simple case is considered, for illustrative purposes. If growth is considered in terms of morphogenetic constraints and development, without taking into account environmental parameters, it can be expressed as a function of the number and mass of cells:

where C is the number of cells in the plant, dependent on the division rate dC/dt in cells d –1 , and m is the mass of organic carbon in each cell, g cell –1 .

As in Equation (4b), this can be partitioned into developmental processes occurring in leaves and in roots, where W L and W R refer to the dry mass of organic carbon in the leaf and root, respectively:


The three perspectives on growth can be unified to show their interrelated nature, and to illustrate the overarching dependence of growth on source–sink relationships. While the physiological perspective focuses on metabolic processes which exchange carbon with the external environment, the allocation perspective focuses on the tissues that carry out net acquisition and drawdown of carbon, and the developmental perspective focuses on the rate of cell division in these tissues, all three perspectives are underpinned by source:sink interactions.

The mass of leaf and root tissues, seen in Equations (4b) and (6b) (relating to physiology and development, respectively), are dependent on allocation and can be expressed as follows:

Substituting for dW P /dt in Equation (6b) using Equation (4b) unifies the physiological and developmental perspectives:

and substituting in the definitions of W L and W R seen in Equations (7a) and (7b) incorporates the allocation perspective, to give:

where the dependence of SLA and LMR on W P has been suppressed for ease of presentation.

This unifies the three lenses for looking at growth, and can be rearranged as:

which is an expression of, for carbon:

Equation (9) illustrates an important point: it is relatively easy in a single mathematical formulation to encapsulate the intrinsic limitations on growth imposed by the physiology of resource capture, internal resource partitioning, and morphogenetic constraints on organ development. Equation (9) is not intended to be a realistic and detailed representation of growth—as discussed, it makes manifold simplifying assumptions and ignores several important components. Rather, it is intended to illustrate the potential value of taking such a unifying approach, as in the more realistic, detailed representations of the plant system developed by Chew et al. (2014) and Evers et al. ( Evers et al. , 2010 ; Vos et al. , 2010 ). This unification is conceptually useful for understanding how the critical processes of source and sink development and activity interact to limit growth in different species. A key step forwards will be model representation of the mechanisms that govern the crosstalk and interactions between different components.

Crucially, Equation (9) shows that source–sink interactions underpin all the aspects of growth described in the preceding equations. A balance between source and sink is essential for plants to grow and develop efficiently. Increased organ initiation, faster cell growth, and larger organ size will strengthen sinks; changes in the root:shoot ratio or leaf area ratio can alter the balance between carbon and nitrogen source and sink tissues; while uptake rates of carbon and mineral nutrients are primary determinants of source strength. A holistic understanding of growth rate should therefore draw on the concepts of source and sink strength, recognizing that each depends on the size and activity of the relevant tissue [Equations (1) and (2)]. Integrating molecular interactions at the tissue level ( Fig. 1 ) with the behaviours of whole plants in terms of physiological regulation, allocation to different tissues and developmental processes will be critical for building a picture of the interactions between the three components discussed above. In order to increase crop yield effectively, it will be essential to build comprehensive growth models in which the source:sink balance is the cornerstone underpinning physiological, allocation-based, and developmental mechanisms for growth limitation. This will create an integrated perspective that allows the effects of this vital determinant of growth to be realized.

An integrated understanding of source–sink relationships, growth, and yield is a vital next step in ongoing efforts to increase crop productivity, and requires a number of key ‘unknowns’ to be addressed: (1) Which components in the plant system of sources and sinks exert the strongest control over growth in major crops? (2) How do these source and sink limitations change during the crops’ lifetimes? (3) Through what developmental or physiological mechanisms do these limitations arise? (4) Via genetic modification or selective breeding, to what extent is it possible to manipulate these processes to upregulate source and sink together, at the appropriate stage of development, to improve crop production?

We advocate the development of an integrated perspective, unifying physiological limitations on fluxes, controls on growth allocation, and the development of sink tissues, to successfully improve crop growth. A holistic view of the mechanistic interactions between sinks and sources is needed at the whole-plant scale during the trajectory of growth and development, in order to identify bottlenecks limiting growth rate. To address this knowledge gap, it will be vital to develop a greater understanding of the physiological processes operating at intermediate scales between molecular mechanisms and whole-plant traits. Ideotypes for future crops have been proposed ( Sreenivasulu and Schnurbusch, 2012 ; Bennett et al. , 2012 ; von Caemmerer et al. , 2012 ; Reynolds et al. , 2012 ; Ort et al. , 2015 ), but reaping the maximum possible gains from these approaches requires a parallel effort in understanding how and when source and sink capacity limit growth and yield.

We thank Professor Andrew Fleming (Department of Animal and Plant Sciences, University of Sheffield) for helpful discussions relating to the manuscript. We are grateful to the three anonymous reviewers who provided constructive and insightful comments that significantly improved the manuscript. We thank Tiffany Bowman (Brookhaven National Laboratory) for assistance with graphic design. AW was supported by a PhD studentship from the Society for Experimental Biology (SEB). AR was supported by the United States Department of Energy contract No. DE-SC00112704 to Brookhaven National Laboratory and by the Next-Generation Ecosystem Experiments (NGEE Tropics) project that is supported by the Office of Biological and Environmental Research in the Department of Energy, Office of Science.

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  • Published: 05 December 2017

Effect of different organic fertilizers application on growth and environmental risk of nitrate under a vegetable field

  • Shuyan Li 1 ,
  • Jijin Li 2 ,
  • Bangxi Zhang 1 , 3 ,
  • Danyang Li 1 ,
  • Guoxue Li 1 &
  • Yangyang Li 1  

Scientific Reports volume  7 , Article number:  17020 ( 2017 ) Cite this article

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  • Environmental sciences

The effect of chicken manure after different disposal methods (water-logged composting, GOF; anaerobic digestion, BR; thermophilic composting, ROF) on vegetable growth and environmental risk was investigated under the tomato-celery-tomato field. Results showed that organic fertilizers significantly increased vegetable yield and quality, but with inappropriate application may cause serious environmental risk such as nitrate pollution. Maximum vegetable yield of 80.9, 68.3, 112.7 t·ha −1 (first, second and third rotation crop, respectively) with best vegetable quality was obtained in ROF treatment. The highest N use efficiency with the least nitrate enrichment in soil was also found in ROF treatment. Moreover, under this fertilization way, nitrate concentration in soil leachate dropped to 6.4 mg·L −1 , which satisfied the threshold (<10 mg·L −1 ) for drinking water set by the US Environmental Protection Agency. Thus, ROF was suggested to be the optimal fertilizer with the best yield, quality and the least environmental risk under the “ tomato-celery” rotation system.


Although nitrogen (N) utilization has generally been optimized in agriculture, unreasonable fertilization can lead to agricultural non-point source pollution 1 , 2 , 3 , 4 , 5 , 6 , and improvements are necessary to avoid adverse environmental impacts of nitrate leaching. Nitrate leaching has a significant influence on plant N supply and groundwater quality. Nitrate concentrations in soil depend on the relation between uptake by plants, soil organisms, atmospheric N 2 fixation, N mineralization (ammonification and nitrification), N deposition from the atmosphere, denitrification, and volatilization 7 .

The development of intensive agricultural areas based on irrigation with groundwater and N application in farming areas has had serious side effects on the land ecosystems including ground water depletion and nitrate leaching to ground water 6 , 8 . Due to environmental pollution, high nitrate concentrations may accumulate in the edible parts of some vegetables, particularly if excessive N fertilizer has been applied 9 . Consuming these crops can harm human health.

Leaching of nitrate from soil is driven by land-use type, management (e.g., fertilization), land-use change, climate, and soil properties 10 . Nitrate-N leaching losses were usually less from fine-textured soils than from coarse-textured soil 11 . The soil nitrate content may higher in spring than in autumn 12 . Precipitation/irrigation can significantly increase the nitrates in the soil leachate 13 , 14 . Nitrate losses decreased with the drain depth decreased 15 .

Organic fertilizers have been proposed as one solution to relieve environmental pressure and be a carbon-neutral alternative to liquid fossil fertilizers 16 . Organic matter improves soil structure, increases the water holding capacity and promotes biological transformations such as N-mineralization 16 , 17 . Several researchers have examined the impact of timing of N and water applications on crop yield in field experiments 8 , 18 . Behnke et al . 19 found that N annual losses from 22.7 to 59.9 kg·ha −1 , and they increase with N fertilization rates increase. The soil NO 3 − -N content under basal fertilizer was 1.65 times higher than that without fertilizer at 0–10 cm on the 36th day after sowing 20 . Davis et al . 21 found that N applications increased N leaching and N 2 O emission without increasing biomass production. Liu et al . 9 found that lettuce augmented with organic fertilizers had significantly longer and wider leaves, higher shoot, and lower NO 3 − -N concentrations compared with the same amount of inorganic fertilizers. Guo et al . 22 found that N fertilizers coupled with farm yard manure resulted in 70% less NO 3 − -N accumulation in the soil profiles than that using mineral N fertilizer alone. However, some researches had found that manure applications without any pretreatment could cause serious NO 3 − -N leaching 23 , 24 .

There have been many kinds of organic fertilizers, such as manure, sewage sludge, stalks, compost, biogas residues, biogas slurry and so on. An increasing body of literature has been focused on the N fertilizers for crop yield and NO 3 − -N leaching, but very little is about comparing different kinds of organic fertilizers on NO 3 − -N distribution (soil, leachate and crop), vegetable yield and quality during the agricultural process. To solve the problem of nitrate content in vegetables, soil and underground water exceeding standard caused by unreasonable fertilization, specific objectives of this study were to: (i) evaluate different organic fertilizers on vegetable yield and quality; (ii) and also determine nitrate concentrations in different soil layers and soil leachate to evaluate environmental risk.

Results and Discussion

Vegetable yield.

As expected, organic fertilizers significantly increased vegetable yield by 7.6–45.2% (Fig.  1 ). For the first rotation, tomato yield increased by 9.2–20.1% compared with CK. Among this, ROF did best with the yield of 84.9 t·ha −1 and it was significantly higher than other treatments. However, GOF had the least effect on tomato yield and BR was similar to GOF with the increase of 9.8%. In the second rotation, all the treatments increased the celery yield by 7.6–8.4%. The maximum increase was ROF treatment with the production of 68.3 t·ha −1 . Compared with tomato, the increase of celery was not obvious. After application of organic fertilizers for one year, the tomato yield in all the treatments in this rotation increased compared with the first rotation. This was mainly due to the higher N mineralization as a result of higher biological activity 25 . For the third rotation crop, tomato yield increased by 25.8–45.2% compared with CK. In this time, ROF has the maximum yield with 112.7 t·ha −1 . Among this “tomato-celery-tomato” system, organic fertilizers significantly increased the vegetable yield according to ANOVA test. This may because organic fertilizer application can increase soil organic matter and then increase yields 26 , 27 .

figure 1

Effect of different organic fertilizers on vegetable yield. Mean differences in the bars are significant at P 0.05 level with different letters. Tomato 1 means the first rotation vegetable; Celery means the second rotation vegetable; Tomato 2 means the third rotation vegetable. Repeat in following figure.

Vegetable quality

Application of organic fertilizers can increase vegetable qualities (Fig.  2 ). The concentration of vitamin C (Vc) after harvest the vegetables is shown in Fig.  2a . Application organic fertilizers significantly increased the concentration of Vc by 3.0–33.5% in the first rotation crop. ROF with the Vc concentration of 122 mg·kg −1 had the best effect and GOF did worst. This may because GOF had a low humification degree without a thermophilic phase 9 . The concentration of Vc increased by 12.6–31.5% in celery planting. Like the first rotation, ROF with the concentration of 83.5 mg·kg −1 had the best effect and GOF had the least effect. After three rotations, Vc of tomato in CK treatment decreased from 91.4 (first rotation) to 79.0 (third rotation) mg·kg −1 , indicating undernourishment and N depletion. Organic fertilizers application could increase the concentration of Vc by 31.6–48.1% compared with CK in the third rotation. ROF with the concentration of 117 mg·kg −1 had the best effect. This is mainly because ROF with a high stabilization and humification degree could improve soil structure, increase the water holding capacity and promote biological transformations and then improve the vegetable quality 9 .

figure 2

Effect of different organic fertilizers on vegetable quality Vc: vitamin C; SE: soluble sugar; TA: titratable acidity.

Figure  2b gives the concentration of soluble sugar (SE) after harvest the vegetables. Application organic fertilizers can significantly increase the concentration of SE by 9.9–17.3% in the first rotation. ROF had the best effect with the concentration of 3.67%. The concentration of SE was increased by 23.6–55.6% in celery planting. ROF with the concentration of 1.12% had the best effect among all the treatments, and GOF had the least effect of all. In the third rotation, the concentration of SE was increased by 18.2–30.3%. Similar to the celery, ROF with the concentration of 4.30% had the best effect of all, and GOF had the least effect. The concentration of SE with the third rotation increased in all treatments including CK compared with the first rotation. This illustrates that long-term application of organic fertilizer can improve the quality of vegetables.

The concentration of titratable acidity (TA) after harvest tomatoes is shown in Fig.  2c . Organic fertilizers application has no significant influence on TA. The content of TA in the third rotation decreased compared with the first rotation, indicating that organic fertilizer can improve the vegetable taste.

Nitrate concentration in vegetable

NO 3 − -N concentration is an important quality characteristic of vegetable. NO 3 − was perceived as a purely harmful dietary component which causes infantile methaemoglobinaemia, carcinogenesis and possibly even teratogenesis 28 . Figure  3 gives the NO 3 − -N concentration in tomato and celery. From this, NO 3 − -N concentrations of the two rotations of tomato were all less than 120 mg·kg −1 especially in the latter, which were far less than the limit of the national standard 600 mg·kg −1 (GB18406.1-2001). Celery is a crop which is easy to enrich NO 3 − and this is why the NO 3 − -N concentration in the third rotation of tomato lower than the first rotation especially in CK treatment. NO 3 − -N concentration in celery was much higher than that in tomato, but it was still less than the limit of the national standard 3000 mg·kg −1 . Tomato-celery rotation system could significantly decrease the vegetable NO 3 − -N concentration under this continuous fertilization field. Through these three rotations, ROF had no significant difference with CK in terms of vegetable NO 3 − -N concentration, which indicates that ROF is a relatively safe way for fertilizing.

figure 3

Effect of different organic fertilizers on nitrate content of tomato and celery.

Nitrate content in soil

Nitrate concentration in the 0–60 cm soil layers (in time).

NO 3 − -N concentration in the root zone soil of the three rotations are shown in Fig.  4 . Organic fertilizers significantly affect the soil nitrate concentration in the top layers (0–60 cm). The NO 3 − -N concentration in the 0–30 cm soil layer of GOF and ROF treatments achieved the minimum value after harvest the second rotation (celery). Celery roots were mainly distributed in 0–30 cm 29 resulting in less absorbing of NO 3 − -N below 30 cm soil layer. This may be the reason why the NO 3 − -N concentration in 30–60 cm soil layer higher than that in 0–30 cm soil layer after harvest celery. Furthermore, for the second rotation NO 3 − -N content in the top 30 cm soil layer reduced by 60–80% compared with the first rotation, but NO 3 − -N in the 30–60 cm soil layer may have a small amount of accumulation for little absorption. However, there were no significant differences in the soil NO 3 − -N content in terms of the whole top layers (0–60 cm) compared with CK, due to NO 3 − -N absorption and enrichment in celery. The soil NO 3 − -N concentration after harvest the first rotation of tomato was significantly higher than the other rotations. This may be caused by the high nitrate content of the original soil (Table  1 ). Organic fertilizers application significantly increased the NO 3 − -N concentration in the 0–30 cm soil layer of all treatments after the first rotation, and especially in BR reached 138.2 g·kg −1 , indicating a high risk of leaching. However, NO 3 − -N in the 30–60 cm soil layer changed slightly due to root absorption. After third rotation, NO 3 − -N concentration was significantly lower than the first rotation, owing to the low nitrate background values in this rotation after harvest celery. In this time, NO 3 − -N concentration in the 0–30 cm soil layer increased slightly. Moreover, NO 3 − -N concentration in the 30–60 cm reduced significantly, which could be attributable to the higher absorption of N in the 30–60 cm soil layer by the deeper root of tomato 30 . Thus in this tomato- celery rotation system, long time application of organic fertilizers will not affect soil nitrate content in the top layers (0–60 cm).

figure 4

Nitrate content in 0–60 cm soil profile after harvest vegetables (with time).

Nitrate content in soil profile (in depth)

Organic fertilizer significantly affected soil NO 3 − -N concentration in the 0–175 cm soil layers (Fig.  5 ). Due to incomplete utilization of fertilizer, treatments with the organic fertilizers increased the nitrate content in soil profile especially in the top layers compared with CK. Topsoil had the most obvious effect, above all GOF treatment reached 29.9 mg·kg −1 , and this may be result from nitrification and mineralization for its instability 20 . Conversely, owing to the higher humification and stability degree of ROF 31 , nitrate content in ROF treatment was lower than any other fertilization treatments. After application of BR and GOF, nitrate had a dramatic enrichment in deep soil (especially below 75 cm) indicating N surplus, and such accumulation of NO 3 − -N in soil profile posed a high risk of N leaching into groundwater. BR and GOF were all incomplete fermentation without thermophilic phase, and then they had a low humification degree with very little stabilized organic matters 32 . Thus a large amount of nitrogen in BR and ROF cannot be fixed like ROF, which lead to nitrate leaching seriously. In ROF treatment, nitrate content in the soil below 100 cm almost had no difference with CK. From the perspective of security, ROF is the environmentally friendly way for fertilizing.

figure 5

Nitrate content in soil profile after harvest the third rotation (with depth).

Nitrogen balance and N translocation

Calculation of N balance is one potentially useful method for predicting the risk of nitrate leaching into groundwater 10 . N balance in each treatment was calculated under this tomato-celery rotation system (Table  2 ). Without fertilizer, the amount of N min could achieve about 145 kg·ha −1 . However, the N residual level was lower than the N initial level, indicating soil N depletion in some degree. N uptake in the fertilization treatments were higher than that in CK treatment, especially in the ROF treatment, showing that fertilization can promote the absorption of N by root. After organic fertilizer application, the residual NO 3 − -N in the 0–60 cm soil layer after crop harvest accumulated to 100–122 kg·ha −1 . Although this was still higher than the environmental safety standard in Europe (90–100 kg·ha −1 in the 0–100 cm soil layer) 10 , it resulted in 50–75% less NO 3 − -N accumulation in the soil profiles than the initial soil, and therefore the environmental risk was reduced in some degree. These results suggested that organic fertilizer application could be benefit for crop uptake, reduce the NO 3 − -N in the soil and then alleviate the soil NO 3 − -N leaching. NUE in these fertilization treatments were 19.4–30.0%, the ROF treatment presented the highest NUE among all the treatments due to the highest uptake by crops, implying the optimum fertilization way.

Nitrate concentration of soil leachate

Although the organic fertilizer application could be benefit for crop uptake and reduce the NO 3 − -N in the soil, soil are still at the high risk of leaching with the high N residual and low NUE in all the fertilization treatments. Then the NO 3 − -N concentration of soil leachate at 100 cm depth below the soil surface were detected after harvest vegetables. NO 3 − -N concentration of soil leachate varied with treatments and crop types, ranging from 6.3 to 35.1 mg·L −1 for tomato and from 4.2 to 30.3 mg·L −1 for celery (Table  3 ). Soil NO 3 − -N leaching in tomato seasons was generally higher than in celery seasons due to higher crop N uptake and higher evaporation in celery rotation leading to less drainage into deeper layers. NO 3 − -N leaching in all treatments decreased after application of organic fertilizers especially ROF. Fertilizer type significantly affects the NO 3 − -N concentration in the soil leachate. The least NO 3 − -N leaching was observed in the ROF treatment mainly due to ROF with a higher organic matter content and biological activity, stabilization and humification degree, resulting in the increase of soil aggregation, nitrogen fixation capacity and decrease of NO 3 − -N leaching 25 . Moreover, NO 3 − -N concentration in CK and ROF treatments dropped below 10 mg·L −1 after harvest the second rotation (celery), which satisfied the threshold (<10 mg·L −1 ) for drinking water set by the US Environmental Protection Agency. This result suggested that application of ROF was no more likely to impair groundwater quality than the GOF, BR or even CK treatments.


Organic fertilizers significantly increased vegetable yield and quality, but with inappropriate application may cause serious environmental risk. Maximum vegetable yield of 80.9, 68.3, 112.7 t·ha −1 (first, second and third rotation crop, respectively) with best vegetable quality was obtained in ROF treatment. The highest N use efficiency with the least nitrate enrichment in soil was also found in ROF treatment. Moreover, under this fertilization way, nitrate concentration in soil leachate satisfied the threshold for drinking water. Thus, ROF was suggested to be the optimal fertilizer with the best yield, quality and the least environmental risk under the “tomato-celery” rotation system.

Materials and methods

Site description.

One and a half years of field experiments (tomato1-celery-tomato2) were conducted on clay loam soil at Liuminying Agricultural Ecological Station (39°41′ N, 116°34′ E) in southeast suburb area (Daxing district) of Beijing, northwest edge of North China Plain. The soil was calcareous, alkaline, and rich in phosphorus and potassium. Agriculture in the area is intensified by a double cropping system (two vegetables a year) with high-yielding cultivar and high inorganic fertilizer (more than 1000 kgN·ha −1 ·yr −1 ) input. Some of the characteristics of this soil were determined before this experiment (Table  1 ). The average air temperature during tomato planting period was about 25 °C, while in celery planting period was about 18 °C.

Crop rotation and experimental fertilizers

A typical spring tomato–autumn celery double cropping rotation was chosen, representative of the common farming practices in the area, where tomato is usually planted from March to July and celery from August to October. Tomato cultivar with Israel 1420 greenhouse grown tomato (Lycopersicon esculentum Mill.) was planted in the experimental plot (see Section 2.3) at a density of 36,000 plant·ha −1 . After tomato harvest, soil was ploughed before planting autumn celery. Celery cultivar with California celery (Apium graveolens L) was planted in the experimental plot at a rate of 2,300,000 plant·ha −1 . The selected crop varieties and planting densities is representative of that used by local farmers.

In order to evaluate of agronomic and ecological effects of soil amendment, three kinds of common organic material i.e. general organic fertilizer (GOF), biogas residue (BR) and refined organic fertilizer (ROF) were used as N fertilizer. GOF was made by chicken manure and corn stalk through water-logged composting; BR was taken from Liuminying Biogas Station, which was made by chicken manure through anaerobic digestion; and ROF was made by chicken manure and mushroom residue through a 90 days thermophilic aerobic composting. Some of the composition and characteristics of these organic fertilizers are given in Table  4 .

Experimental design

The experiment was conducted in a vegetable greenhouse during the tomato and celery growing season. Four treatments with three replicates were carried out, namely CK, GOF, BR and ROF. Then the experimental area consisted of 12 plots, 5.5 m wide and 6 m long for each, and these 12 plots were arranged as split plots in a randomized complete block with a 0.5 m isolation strip in order to avoid interference. The CK was a control treatment without fertilization. GOF, BR and ROF treatments were applied with the same amount of N with 350 kgN·ha −1 for each crops. Previous study has found that top dressing can increase the crop yield 20 . Then in this experiment, 66.7% of the fertilizer was used as base fertilizer and the remaining 33.3% as top dressing in fruit swelling period and vigorous period for tomato and celery, respectively. The management practices for controlling pest, disease and weeds complied with local practices for high-yield production.

Analytical methods

Tomato and celery plant were sampled from a 5 m 2 area in each plot at harvest for the measurements of vegetable (tomato and celery) yield and tomato residual biomass. Samples of vegetable and tomato residual were oven-dried at 65 °C until they reached a constant weight to determine the water content and dry matter. The N content in vegetable and tomato residual of the samples were determined by the micro-Kjeldahl method by digesting the sample in H 2 SO 4 -H 2 O 2 solution 33 . N uptake by plants was estimated by multiplying the tomato, tomato residual and celery dry matter weight by their N concentrations.

Three tomatoes (or three plants of celery) per plot with similar degree of maturity and similar size and without external defects were picked for the quality indices (mainly taste quality, nutrient quality and safety quality) measurement. Tomatoes or celeries were squeezed in a blender, and then the content of vitamin C (Vc), soluble sugar (SE), and titratable acidity (TA) in the plants were detected according to 34 . Besides, some of the squeezed vegetable was extracted with deionized water, filtered and then the concentration of NO 3 − -N in vegetable was determined by a continuous-flow analyzer (TRAACS 2000, Bran and Luebbe, Norderstedt, Germany).

For soil N measurements, three ceramic candle extraction systems with tubes (inside diameter 50 mm) were installed in each plot at 100 cm soil depths. The amount of nitrate leached during the growing season may be minimal compared to leaching losses that occur between the harvest of one crop and the planting of the next 23 . Then samples of the soil leachate were taken after each harvest and/or before sowing. Furthermore, soil samples in all plots were taken after each harvest and/or before each planting by sampling three cores per plot with an auger (3 cm inside diameter tube) to 60 cm depth in 30 cm increments. Moreover, soil samples in the depth of 15, 45, 75, 125 and 175 cm were taken after harvesting the second batch of tomato (tomato 2) to research the change of nitrate with soil depth. Soil samples obtained from the same layer and plot were thoroughly mixed. All of the soil and soil leachate samples were immediately brought to the laboratory for the measurement of NO 3 − -N and soil moisture content.

Each fresh soil sample was extracted with CaCl 2 35 , and the concentration of nitrate was determined by a continuous-flow analyzer (TRAACS 2000, Bran and Luebbe, Norderstedt, Germany). Soil samples were dried to a constant weight in an oven at 105 °C to determine the water content and dry matter. Bulk density of the soils was measured in the 0–60 cm soil depth with soil cores (3 cm inside diameter by 20 cm long). The NO 3 − -N contents in soil (mg·kg −1 ) were converted to kg·ha −1 based on the bulk density of different soil layers in order to calculate the N balance. For the nitrate analysis of soil leachate, the water samples were filtered through 0.45 μm membranes and the concentration of nitrate was determined by a continuous-flow analyzer 36 .

Nitrogen balance

Items in the N balance were estimated in each plot during the whole crop growing seasons. NO 3 − -N below 60 cm soil depth and NH 4 + -N throughout the soil profile will not be included in the N balance calculations because the crop roots in this experiment were mainly distributed in the 0–60 cm depth and relatively low changes in NH 4 + -N content between seasons were found (data not presented). The N balance can be written as:

where N initial is initial soil NO 3 − -N in the 0–60 cm soil profiles; N input is N application rate (350 kg N·ha −1 per rotation crop plus 3 rotation crops); N min is N mineralization; N uptake is N uptake by plant; N residual is residual NO 3 − -N in 0–60 cm soil profiles, and N surplus represent N that store in various soil fraction (mainly organic N) and N loss. N loss is considered as mainly NO 3 − -N leaching, since other N losses via denitrification, volatilization and erosion are relatively low under such environmental conditions as reported by Fang et al . 37 .

N mineralization (N min ) was estimated by the balance of N inputs and outputs in the control (CK) as follows:

where N uptake,0 , N residual,0 and N initial,0 are crop N uptake, residual and initial soil NO 3 − -N in the 0–60 cm soil profile of the control, respectively.

N utlization is the part of N uptake offered by organic fertilizer. NUE is the fertilizer N use efficiency during the one and a half years of experiment period.

Statistical analyses

Analysis of variance (ANOVA) was performed with the SAS8.2 for Windows, and mean comparisons were done using the least significant difference (LSD) test at P < 0.05.

Data availability statement

The authors declared that none of the data in the paper had been published or was under consideration for publication elsewhere.

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This research was financially supported by the High Effective Intelligent Composting Process and Key Technology Research (2016YFD0800600-01) and the Research Project for Technical System Construction in Cashmere Goat Industry of Ministry of Agriculture of the People’s Republic of China (CARS-39-19).

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Shuyan Li, Bangxi Zhang, Danyang Li, Guoxue Li & Yangyang Li

Institute of Plant Nutrition and Resources, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China

Guizhou Institute of Soil and Fertilizer, Guiyang, 550006, China

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J.L., G.L. and S.L. designed the experiment, S.L., B.Z., D.L., and Y.L. performed the experiment and did the statistical analysis, S.L. wrote the first draft of the manuscript.

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Li, S., Li, J., Zhang, B. et al. Effect of different organic fertilizers application on growth and environmental risk of nitrate under a vegetable field. Sci Rep 7 , 17020 (2017).

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Received : 04 August 2017

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A Review of Elevated Atmospheric CO 2 Effects on Plant Growth and Water Relations: Implications for Horticulture

Empirical records provide incontestable evidence for the global rise in carbon dioxide (CO 2 ) concentration in the earth's atmosphere. Plant growth can be stimulated by elevation of CO 2 ; photosynthesis increases and economic yield is often enhanced. The application of more CO 2 can increase plant water use efficiency and result in less water use. After reviewing the available CO 2 literature, we offer a series of priority targets for future research, including: 1) a need to breed or screen varieties and species of horticultural plants for increased drought tolerance; 2) determining the amount of carbon sequestered in soil from horticulture production practices for improved soil water-holding capacity and to aid in mitigating projected global climate change; 3) determining the contribution of the horticulture industry to these projected changes through flux of CO 2 and other trace gases (i.e., nitrous oxide from fertilizer application and methane under anaerobic conditions) to the atmosphere; and 4) determining how CO 2 -induced changes in plant growth and water relations will impact the complex interactions with pests (weeds, insects, and diseases). Such data are required to develop best management strategies for the horticulture industry to adapt to future environmental conditions.

The level of CO 2 in the atmosphere is rising at an unprecedented rate, has increased from ≈280 ppm at the beginning of the industrial revolution (≈1750) to ≈380 ppm today, and is expected to double preindustrial levels sometime during this century ( Keeling and Whorf, 2001 ; Neftel et al., 1985 ). This global rise can be primarily attributed to fossil fuel burning and land use change associated with industrial and/or population expansion ( Houghton et al., 1990 ). This rise, along with other trace gases, is widely thought to be a primary factor driving global climate change ( IPCC, 2007 ). Aside from the debate on anthropogenic-driven climate change, vegetation will be directly impacted and research has shown that plants respond positively to elevated CO 2 ( Amthor, 1995 ). Most of this research has focused on agricultural and forest species with limited work on specialty crops associated with horticulture. Horticulture is a diverse industry (encompassing many small businesses) that impacts the landscape of both rural and urban environments and has an economic impact of $148 billion annually in the United States ( Hall et al., 2005 ). We will attempt to discuss the effects of the rise in atmospheric CO 2 concentration on plant growth and water relations with a focus toward implications for horticultural production systems with suggestions for future research areas.

Carbon dioxide links the atmosphere to the biosphere and is an essential substrate for photosynthesis. Elevated CO 2 stimulates photosynthesis leading to increased carbon (C) uptake and assimilation, thereby increasing plant growth. However, as a result of differences in CO 2 use during photosynthesis, plants with a C 3 photosynthetic pathway often exhibit greater growth response relative to those with a C 4 pathway ( Amthor, 1995 ; Amthor and Loomis, 1996 ; Bowes, 1993 ; Poorter, 1993 ; Rogers et al., 1997 ). The CO 2 -concentrating mechanism used by C 4 species limits the response to CO 2 enrichment ( Amthor and Loomis, 1996 ). For C 3 plants, positive responses are mainly attributed to competitive inhibition of photorespiration by CO 2 and the internal CO 2 concentrations of C 3 leaves (at current CO 2 levels) being less than the Michaelis-Menton constant of ribulose bisphosphate carboxylase/oxygenase ( Amthor and Loomis, 1996 ). Although increased photosynthesis under elevated CO 2 enhances growth for most plants, summaries have consistently shown that this increase varies for plants with a C 3 (33% to 40% increase) versus a C 4 (10% to 15% increase) photosynthetic pathway ( Kimball, 1983 ; Prior et al., 2003 ).

Given that most horticulture species have a C 3 pathway, it is expected that they will show similar responses to elevated CO 2 . Early work ( Cummings and Jones, 1918 ) demonstrated that both vegetable and flower crops benefited from above ambient concentrations of CO 2 ; both cyclamens and nasturtiums showed increased dry weight and greater flower yield when exposed to elevated CO 2 . Since this early work, others have shown that ornamental species respond positively to elevated levels of CO 2 ( Davis and Potter, 1983 ; Gislerød and Nelson, 1989 ; Mattson and Widmer, 1971 ; Mortensen, 1987 , 1991 ; Mortensen and Gislerød, 1989 ; Mortensen and Moe, 1992 ; Mortensen and Ulsaker, 1985 ). In fact, increasing the concentration of CO 2 in glasshouses is an economically efficient method of enhancing growth of ornamental and vegetable crops ( Mastalerz, 1977 ; Mortensen, 1987 ).

In addition to stimulating photosynthesis and aboveground growth, elevated CO 2 can alter C partitioning/allocation. Increased C supply from elevated atmospheric CO 2 can preferentially induce the distribution of photosynthate belowground ( Ceulemans and Mousseau, 1994 ; Lekkerkerk et al., 1990 ; Prior et al., 1997 ; Rogers et al., 1994 ). In many cases, the largest proportion of the extra biomass produced under elevated CO 2 is found belowground ( Rogers et al., 1994 ; Wittwer, 1995 ), often resulting in increased root-to-shoot ratio ( Rogers et al., 1996 ). This is not surprising in that plants tend to allocate photosynthate to tissues needed to acquire the most limiting resource ( Chapin et al., 1987 ); when CO 2 is elevated, the most limiting resource becomes water or nutrients.

Although less studied than aboveground response, plants often show increased rooting under CO 2 enrichment ( Chaudhuri et al., 1986 , 1990 ; Del Castillo et al., 1989 ; Rogers et al., 1992 ). In addition to this early work with plants in containers, increased rooting has also been observed in the field using both open-top field chambers (OTC) and free-air CO 2 enrichment systems (FACE). Elevated CO 2 increased dry weight of root systems for both soybean (44%) and sorghum (38%) growing in OTC ( Prior et al., 2003 ). Prior et al. (1994) also found increases in cotton fine roots (dry weight and length) under FACE and that these plants had proportionately more of their roots allocated away from the row center. Furthermore, Prior et al. (1995) reported that these FACE cotton plants had larger taproots and increases in the number and size of lateral roots. The development of more robust root systems in CO 2 -enriched environments may allow for greater carbohydrate storage and infers greater exploration of the soil for resources such as water and nutrients to meet plant growth needs during periods of peak demand such as boll development and filling.

In addition to increases in rooting, colonization of roots with mycorrhizae (the symbiotic association of plant roots with fungi) has been shown to increase under elevated CO 2 ( Norby et al., 1987 ; O'Neill et al., 1987 ; Runion et al., 1997 ). Mycorrhizae increase nutrient uptake by their host plants ( Abbott and Robson, 1984 ), provide additional water to plants through hyphal proliferation in soil ( Luxmoore, 1981 ), and protect roots from pathogenic microorganisms ( Marx, 1973 ).

Because horticultural plants are generally grown in containers without resource limitations (i.e., water and nutrients), increased root growth or mycorrhizal colonization may not become critical for survival and growth until after outplanting into the landscape. However, as a result of limited rooting space, growth in containers has been shown to dampen the response to CO 2 enrichment ( Arp, 1991 ). For plants to use a higher level of atmospheric CO 2 , they must have a means of storing the additional carbohydrates produced. We have shown that plants with a tuberous or woody root system tend to respond to CO 2 enrichment to a greater degree than plants with smaller or more fibrous root systems ( Rogers et al., 1994 ; Runion et al., 2010 ). The limited rooting volume experienced by plants growing in containers may help explain the fact that increased growth of horticultural species under elevated CO 2 is sometimes slightly lower than that generally observed for other C 3 plants, falling in the range of 15% to 25% ( Mortensen, 1991 , 1994 ). Nonetheless, the increased biomass production under high CO 2 should be advantageous for horticultural plants in that they should attain a marketable size more rapidly.

In addition to the effects of CO 2 on photosynthesis and C allocation mentioned, elevated CO 2 can impact growth through improved plant water relations ( Rogers and Dahlman, 1993 ). In fact, most plants (both C 3 and C 4 species) exhibit improved plant water relations. Elevated CO 2 slows transpiration by inducing the partial closure of leaf stomatal guard cells ( Jones and Mansfield, 1970 ). Studies in growth chambers and glasshouses have shown that elevated CO 2 reduces transpiration for both C 3 ( Allen et al., 1994 ; Jones et al., 1984 , 1985 ; Pallas, 1965 ; Prior et al., 1991 ; Valle et al., 1985 ) and C 4 ( Chaudhuri et al., 1986 ; Pallas, 1965 ; Van Bavel, 1974 ) plants. Dugas et al. (1997) , using stem flow gauges under actual field conditions, also showed that whole-plant transpiration was reduced under elevated CO 2 for both a soybean (C 3 ) and a sorghum (C 4 ) crop.

This reduction in transpiration, coupled with increased photosynthesis, can contribute to increased water use efficiency (WUE = the ratio of carbon fixed to water transpired), which has often been reported ( Baker et al., 1990 ; Morison, 1985 ; Sionit et al., 1984 ). In fact, Kimball and Idso (1983) cited 46 observations that cumulatively showed that transpiration would be lowered by an average of 34%, which, coupled with an economic yield enhancement of 33% (over 500 observations), suggested a doubling of WUE for a doubling of CO 2 level. From a physiological standpoint, increased WUE may represent one of the most significant plant responses to elevated CO 2 ( Rogers et al., 1994 ).

Plants with a C 4 photosynthetic pathway show a smaller response to elevated CO 2 than plants with a C 3 pathway. However, both C 3 and C 4 plants show reduced transpiration under elevated CO 2 . Therefore, WUE should be primarily controlled by transpiration in C 4 plants, whereas both are important in C 3 plants. This was demonstrated by Acock and Allen (1985) using data from Valle et al. (1985) and Wong (1980) . In a more recent long-term field study, similar calculations showed contributions of 74% and 26% (for photosynthesis and transpiration, respectively) in soybean compared with respective contributions of 42% and 58% in sorghum ( Prior et al., 2010a ). Although photosynthesis still dominated WUE increase in C 3 soybean, relative contributions of the two processes were more similar for C 4 sorghum than that reported by Acock and Allen (1985) .

Given the fact that elevated CO 2 can reduce transpiration, it has been suggested that this might partially ameliorate the effects of drought ( Bazzaz, 1990 ) and allow plants to maintain increased photosynthesis. This has frequently been observed ( Acock and Allen, 1985 ; Gifford, 1979 ; Goudriaan and Bijlsma, 1987 ; Nijs et al., 1989 ; Rogers et al., 1984 ; Sionit et al., 1981 ; Wong, 1980 ); however, it should be noted that much of this work was conducted in growth chambers and glasshouses using plants growing in containers. Working with container-grown soybean in field OTC, Prior et al. (1991) reported that, at elevated levels of CO 2 , xylem pressure potential of water-stressed plants was equivalent to that of adequately watered plants, indicating amelioration of drought stress.

It has been suggested that in more natural environments, although instantaneous WUE is increased, whole-plant water use may be differentially affected as a result of increased plant size. Allen (1994) reported that larger plant size [higher leaf area index (LAI)] counterbalanced the reduction in water use, offsetting enhanced WUE. Jones et al. (1985) showed that, although elevated CO 2 increased WUE for plants with both a high and a low LAI, this increase was greater for plants with a lower LAI. Working with longleaf pine growing in large (45 L) containers, we found that nitrogen (N) availability was also an important factor affecting the interaction of WUE and plant water stress ( Runion et al., 1999 ). Longleaf pine seedlings grown with adequate N grew larger under elevated CO 2 , resulting in increased whole-plant water use and increased water stress despite increased WUE. Seedlings grown with limited N did not exhibit a growth response to elevated CO 2 , so the increased WUE resulted in decreased whole-plant water use and reduced stress.

In addition to improved plant water relations, elevated CO 2 can also affect water movement through the landscape. Water infiltration can be increased and sediment loss through runoff can be decreased in high CO 2 environments ( Prior et al., 2010b ). These improvements can result from increased plant rooting (as noted previously) and from changes in soil physical properties. Elevated CO 2 can increase soil C, aggregate stability, and hydraulic conductivity and decrease soil bulk density ( Prior et al., 2004 ). These improvements in soil/water relations will be particularly important for horticultural plants in the landscape.

Water is also a crucial resource in many horticultural production facilities and its conservation is becoming an increasingly important issue. The fact that elevated CO 2 can increase plant WUE ( Rogers et al., 1994 ) may indicate that plants could be watered less frequently as CO 2 levels continue to rise. However, because these plants are generally grown with optimal nutrients, elevated CO 2 may increase plant size to a point where watering frequency will need to be maintained at current levels or even increased. This interaction of elevated CO 2 and resource availability will also be of critical importance for horticultural species after outplanting to the landscape where periodic droughts could be relatively frequent. The landscape's response may not be adequately reflected by studies of small numbers of plants grown in containers; obviously, more work is needed within this important industry to maximize plant growth, health, and efficient use of resources.

Although much is known regarding the effects of elevated CO 2 on plants, horticultural species have received much less attention than agronomic and forest species. Although it is likely that most horticultural species will benefit (through increased growth) from rising CO 2 , research to support this contention is lacking. Horticulture comprises diverse species in terms of growth forms (e.g., annuals, perennials, trees, shrubs, forbs, grasses, vegetables, floriculture crops, C 3 , C 4 ) and the conditions in which they are grown (e.g., container versus in-ground, indoor versus outdoor). Knowledge of how these diverse plant types will respond to elevated CO 2 under current growing conditions would be valuable in terms of adapting management strategies to future environmental conditions. For example, although container-grown plants are known to respond positively to elevated CO 2 in terms of increased growth, it is also known that root restriction can dampen this CO 2 response; therefore, it is important to determine optimal container sizes for producing marketable plants on timely schedules.

As noted previously, positive growth responses to elevated CO 2 result not only from increased uptake and assimilation of CO 2 , but also from decreased transpiration, which improves plant water relations and WUE. Water conservation is a critical issue for crop production, particularly in certain regions of the United States. Within the horticulture industry, adjustments to watering frequency may become a crucial management decision. Knowledge of the effects of rising CO 2 on whole-plant water use will aid managers in optimizing irrigation schedules and amounts.

In addition to understanding the effects of rising CO 2 on water use of currently grown horticultural species, it is important for the industry to breed or screen for varieties and species with higher degrees of drought tolerance. It will also be important that these efforts be conducted at current and future levels of atmospheric CO 2 to select plants that show large responses to elevated levels of CO 2 . One predicted outcome of global climate change is alterations in precipitation patterns with more extreme weather events, including droughts ( IPCC, 2007 ). It is crucial to the industry that plants survive after outplanting in residential and commercial landscape environments.

One means of improving survivability is through use of mulch to conserve soil water. In an agronomic setting, cover crops used in no-tillage management systems can act as mulch ( Balkcom et al., 2007 ). We have shown that these cover crops increase soil C ( Prior et al., 2005 ) and aid in the improvement of soil physical properties ( Prior et al., 2004 ), which also improves soil water relations ( Prior et al., 2010b ). Mulch (commonly pine bark, pine straw, or wood chips in the southeastern United States) contains high concentrations of plant organic C and, when used in landscape settings, can contribute to soil C sequestration. However, the extent of this contribution is not currently known, locally, regionally, or nationally. Furthermore, depending on the fate of these materials (e.g., left on site, burned on site, or used as a fuel source at forest products mills), the potential net increase in soil C from using these materials in landscape settings is also largely unknown.

In addition to mulch, the horticulture industry adds to soil C content through burial of container media at the time of outplanting. In container-grown plant production of nursery crops, plants are grown in a predominantly pine bark-based substrate. Pine bark is composed almost entirely of organic C, having a C content greater than 60% ( Simmons and Derr, 2007 ). When these plants are outplanted to the landscape, this represents a very large amount of C possibly being sequestered in soil. Carbon can also be sequestered in plant biomass through positive growth responses to rising CO 2 . However, to date, little is known concerning the C sequestration potential of the horticulture industry as a whole; this is critical to assess its potential contribution to mitigating potential climate change.

The C sequestration potential of the horticulture industry will be affected by the C:N ratio of inputs from biomass, mulch, and container media. The C:N ratio of these inputs can be high, suggesting slow decomposition and, therefore, slow release of CO 2 back to the atmosphere, aiding mitigation of global climate change. At present, the amount of C added to soil through outplanting container-grown horticultural plants is largely unknown. There is also little knowledge of the residence time of these materials in soil and of the rate of soil CO 2 flux back to the atmosphere. This knowledge will be crucial to determining the C sequestration potential of the horticulture industry and its contribution to potential global climate change through flux of CO 2 from soil to air.

There is also little information on the flux of other trace gases (nitrous oxide and methane) in these systems. Horticulture production facilities often use large amounts of water in irrigation as well as large amounts of fertilizers; this combination of resources could result in substantial fluxes of other gases. Like with CO 2 flux, this information is critical to determining the industry's potential contribution to climate change. It is also necessary to develop best management strategies that minimize trace gas flux, maximize resource use efficiency, and optimize growth and economic gain.

Another largely unknown but important consideration of rising CO 2 will be management of pests (weeds, insects, and diseases) in these systems. Weeds often show greater growth responses to elevated CO 2 than do crop plants, which may be the result of weeds having greater genetic diversity and physiological plasticity than managed plants ( Ziska and Runion, 2007 ). How rising CO 2 will impact weed management strategies in horticultural systems is unknown. The interactions of plants with both insects and diseases are complex and vary according to the host–pest system of interest; however, these interactions have received very little attention ( Ziska and Runion, 2007 ). More knowledge in this area is required to develop best management strategies to deal with these potentially serious threats to productivity and profitability not only in horticulture, but for agriculture and forestry as well.

In general, elevated CO 2 increases plant growth (both above- and belowground) and improves plant water relations (reduces transpiration and increases WUE). It is likely these benefits will also occur for horticultural plants, but data to support this are lacking relative to crop and forest species. In addition to basic research on the response of diverse horticultural species to future levels of atmospheric CO 2 , it may become crucial to breed or screen varieties and species of horticultural plants for increased drought tolerance as a result of predicted changes in precipitation patterns. It is also important to determine the amount of C sequestered in soil from horticulture production practices not only for improvement of soil water-holding capacity, but also to aid in mitigation of projected global climate change. Furthermore, determining the contribution of the horticulture industry to these projected changes through flux of CO 2 and other trace gases (through irrigation and fertilization) is of critical importance. How CO 2 -induced changes in plant growth and water relations will impact the complex interactions with pests (weeds, insects, and diseases) is a deficient area of research not only for horticulture, but for plants in general. All this information is needed to develop best management strategies for the horticulture industry to successfully adapt to future environmental change.

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Contributor Notes

This work was supported by the USDA-ARS, Floriculture and Nursery Research Initiative.

We thank Barry Dorman for technical assistance.

This paper was part of the colloquium “Water Management and Plant Performance in a Changing Climate” held 4 Aug. 2010 at the ASHS Conference, Palm Desert, CA, and sponsored by the Water Utilization and Plant Performance in a Changing Climate (WUM) Working Group.

1 To whom reprint requests should be addressed; e-mail [email protected] .


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Application of ethanol alleviates heat damage to leaf growth and yield in tomato.

Daisuke Todaka

  • 1 Plant Genomic Network Research Team, RIKEN Center for Sustainable Resource Science, Yokohama, Kanagawa, Japan
  • 2 Agricultural Genetics Institute, Hanoi, Vietnam
  • 3 Plant Epigenome Regulation Laboratory, RIKEN Cluster for Pioneering Research, Wako, Saitama, Japan
  • 4 Metabolomics Research Group, RIKEN Center for Sustainable Resource Science, Yokohama, Kanagawa, Japan
  • 5 Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan
  • 6 Tsukuba Plant Innovation Research Center, University of Tsukuba, Tsukuba, Ibaraki, Japan
  • 7 Faculty of Agriculture, Ryukoku University, Otsu, Shiga, Japan
  • 8 Institute for Advanced Biosciences, Keio University, Yamagata, Japan
  • 9 Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan
  • 10 Kihara Institute for Biological Research, Yokohama City University, Yokohama, Kanagawa, Japan
  • 11 Graduate School of Science and Engineering, Saitama University, Saitama, Saitama, Japan

Chemical priming has emerged as a promising area in agricultural research. Our previous studies have demonstrated that pretreatment with a low concentration of ethanol enhances abiotic stress tolerance in Arabidopsis and cassava. Here, we show that ethanol treatment induces heat stress tolerance in tomato ( Solanum lycopersicon L.) plants. Seedlings of the tomato cultivar ‘Micro-Tom’ were pretreated with ethanol solution and then subjected to heat stress. The survival rates of the ethanol-pretreated plants were significantly higher than those of the water-treated control plants. Similarly, the fruit numbers of the ethanol-pretreated plants were greater than those of the water-treated ones. Transcriptome analysis identified sets of genes that were differentially expressed in shoots and roots of seedlings and in mature green fruits of ethanol-pretreated plants compared with those in water-treated plants. Gene ontology analysis using these genes showed that stress-related gene ontology terms were found in the set of ethanol-induced genes. Metabolome analysis revealed that the contents of a wide range of metabolites differed between water- and ethanol-treated samples. They included sugars such as trehalose, sucrose, glucose, and fructose. From our results, we speculate that ethanol-induced heat stress tolerance in tomato is mainly the result of increased expression of stress-related genes encoding late embryogenesis abundant (LEA) proteins, reactive oxygen species (ROS) elimination enzymes, and activated gluconeogenesis. Our results will be useful for establishing ethanol-based chemical priming technology to reduce heat stress damage in crops, especially in Solanaceae.

1 Introduction

Heat stress is one of the most serious problems in agriculture. A recent report by Intergovernmental Panel on Climate Change (IPCC) 2022 shows that the average global surface air temperature in 2030s will be 1.5°C higher than the average in 1850-1900 ( Pörtner et al., 2022 ). The frequency of heat stress conditions has increased with global climate change. Heat stress decreases crop productivity, leading to negative impacts on society and the economy. Therefore, enhancing the heat stress tolerance of crops is an important goal for plant researchers.

Chemical priming is one of the useful techniques that can increase the stress tolerance of plants ( Savvides et al., 2016 ; Sako et al., 2021b ). A wide variety of chemical compounds can elicit molecular mechanisms governing environmental stress tolerance ( Savvides et al., 2016 ; Sako et al., 2021b ; Zulfiqar et al., 2022 ). In the practical use of chemical priming in agriculture, it is important to optimize the method for each situation. For different crop species, for example, the application of different concentrations of the chemical priming compound will be critical for achieving the desired physiological traits.

Recent studies have confirmed that application of ethanol to plants can enhance environmental stress tolerance. We previously showed that ethanol treatment enhanced heat stress tolerance in Arabidopsis through the activated unfolded protein response (UPR) mechanism ( Matsui et al., 2022 ). Ethanol-treated Arabidopsis plants also showed enhanced drought tolerance through activated stomatal closure and gluconeogenesis ( Bashir et al., 2022 ). In addition, ethanol treatment enhanced drought tolerance in wheat and rice ( Bashir et al., 2022 ), soybean ( Rahman et al., 2022 ) and cassava ( Vu et al., 2022 ), salt stress tolerance in Arabidopsis and rice ( Nguyen et al., 2017 ) and soybean ( Das et al., 2022 ), and high-light stress tolerance in Arabidopsis ( Sako et al., 2021a ). Ethanol is readily available and is considered to be environment- and human-friendly. From these perspectives, it is expected that farmers might prefer ethanol chemical priming over other chemical options, and ultimately social acceptance of the method is likely.

Heat stress damages plant growth and yield ( Hoshikawa et al., 2021 ; Ahmad et al., 2022 ). Extensive research has elucidated how photosynthesis is highly sensitive to heat stress ( Hu et al., 2020 ). The damaged photosynthetic processes include electron transport, CO 2 assimilation, chlorophyll biosynthesis, and thylakoid membrane fluidity ( Hu et al., 2020 ). Impaired photosynthesis leads to growth retardation. Heat stress also causes oxidative damage by reactive oxygen species (ROS) such as superoxide radical, singlet oxygen, hydroxyl radical and hydrogen peroxide ( Fortunato et al., 2023 ). To cope with ROS molecules, organisms activate specific enzymes that reduce or inactivate ROS, including peroxidase, ascorbate peroxidase, glutathione reductase, superoxide dismutase, and catalase. Under severe heat stress conditions, proteins are denatured and functionally damaged. Heat shock proteins (HSPs) are induced by high temperatures and protect against protein denaturation through transcriptional cascades ( Ohama et al., 2017 ).

Tomato ( Solanum lycopersicum L.) is one of the most valuable vegetable crops because the fruit contains important nutrients for humans, such as vitamin A, vitamin C and lycopene. Tomato is also a representative species in the Solanaceae family. The plant has been used extensively in research. In particular, the model tomato cultivar ‘Micro-Tom’ has been widely studied. The superiority of ‘Micro-Tom’ is evident in its short generation time, small genome size, and stable genetic modification ( Meissner et al., 1997 ). Genome-wide full-length cDNAs ( Aoki et al., 2010 ) and the complete genome sequence ( Kobayashi et al., 2014 ) of ‘Micro-Tom’ are available.

In the case of tomato, there have been no previous reports that ethanol priming can improve plant growth performance or survival under environmental stress conditions. In addition, little is known about the effects of ethanol treatment on fruit quality in crops. In this paper, we investigated whether ethanol application enhances heat stress tolerance in tomato ‘Micro-Tom’. We show that ethanol pretreatment alleviated heat damage to both vegetative growth and reproductive development. Transcriptome analysis identified the genes differentially expressed between water- and ethanol-treated seedlings and fruits. Furthermore, metabolome analysis unraveled the dynamics of changes in metabolites following ethanol application. Our results give new insight into ethanol-mediated heat stress tolerance in tomato and improve the understanding of such mechanisms more widely in plants.

2 Materials and methods

2.1 plant materials and growth conditions.

Seeds of tomato ( Solanum lycopersicum L.) cultivar ‘Micro-Tom’ were obtained from the National Bioresource Project (MEXT, Japan) through the TOMATOMA database ( Saito et al., 2011 ). Tomato seeds were imbibed in tap water at 22°C overnight under dark conditions. The imbibed seeds were sown into pots (70 mm diameter, 60 mm height, Yamato Plastic Co., Ltd., Nara, Japan) containing water-retaining horticultural clay granules (Seramis, Westland Horticulture Ltd. Tyrone, UK). After sowing, the pots were placed in a growth room set at 22°C with a 16-h light (110 to 140 µmol m −2 s −1 photosynthetic photon flux density)/8-h dark cycle.

2.2 Ethanol pretreatment and heat stress treatment

Sixteen-day-old plants grown in pots were used for ethanol pretreatment. The bottoms of the pots were placed in ethanol solution for 3 d. We selected 20 mM concentration of ethanol in pretreatment solution. This is based on the result of Arabidopsis and lettuce plants ( Matsui et al., 2022 ). After ethanol pretreatment, the pots were placed in an air incubator (Sanyo incubator MIR 153, Sanyo Electric Co. Ltd, Osaka, Japan) set at 50 °C and maintained for the indicated time periods as heat stress treatment. During the heat treatment, the pots were electrically rotated in the air incubator to avoid location effects. After the heat treatment, the pots were returned to the growth room and maintained for the indicated time periods.

2.3 Estimation of green leaf areas

Green leaf areas were estimated by OpenCV (version 4.0.1) on Python 3.8.5. Photographs were taken above each plant. The hue, saturation, and value (HSV) color threshold range was set from [31, 70, 10] to [95, 255, 255].

2.4 Quantitative PCR

Six biological replicates for each treatment were used. One replicate of shoot or root samples consisted of three leaves or one root from one plant, respectively. Samples were put into a 10-mL tube, frozen in liquid nitrogen, and pulverized using a Multi-Beads Shocker system (Yasui Kikai, Osaka, Japan). Total RNA extraction, cDNA synthesis and PCR were performed as previously described ( Matsui et al., 2022 ). Primer sequences are shown in Supplementary Table S1 .

2.5 Transcriptome analysis

For the RNA-seq analysis, the sequencing library was prepared using the Lasy-Seq method ( Kamitani et al., 2019 ). Specifically, 200 ng of total RNA was used per sample. The library was sequenced using the 151-bp paired-end mode of the HiSeq X Ten (Illumina, San Diego, CA, USA). RNA-seq analyses were performed with R1 reads. Low-quality reads and adapters were trimmed using Trimmomatic version 0.39 ( ) with settings ‘ILLUMINACLIP : TruSeaq3-SE.fa:2:30:10 LEADING:3 TRAILING:3 SLIDINGWINDOW:4:15 MINLEN:36’. HISAT2 ( ) version 2.2.1 was used to map the reads to the Solanum lycopersicum SL4.0 reference genome with the ‘–max-intronlen 5000’ option. Aligned reads within gene models were counted using featureCounts version 2.0.1 ( ) with the ‘–fracOverlap 0.5 -O -t gene -g ID -s 1 –primary’ options. Differentially expressed genes were identified using R version 4.0.4 ( ) and DESeq2 version 1.30.1 ( ) package. Genes with false discovery rate < 0.05 in each comparison were identified as differentially expressed. Gene ontology enrichment analysis was performed on the web tool ( ).

2.6 Metabolome analysis by gas chromatography–time of flight/mass spectrometry

GC–TOF/MS analysis was carried out using the procedures described previously ( Jonsson et al., 2005 ; Kusano et al., 2007a ; Kusano et al., 2007b ; Redestig et al., 2009 ) with slight modifications. Approximately 20 mg fresh weight of tissue per mL extraction medium containing ten stable isotope reference compounds was used in the extraction of metabolites.

3.1 Effects of ethanol pretreatment on heat stress tolerance in tomato seedlings

Previously, we found that pretreatment with high concentrations of ethanol decreased shoot growth in Arabidopsis ( Matsui et al., 2022 ). Therefore, we checked whether the 20 mM concentration of ethanol adversely affected shoot growth in tomato. The green leaf area of seedlings pretreated with 20 mM ethanol for 3 d and 6 d were not significantly different from those of the control seedlings pretreated with water ( Supplementary Figure S1 ). These results suggested that 20 mM ethanol treatment did not inhibit shoot growth in tomato and so we proceeded to use that concentration in ethanol pretreatments of tomato thereafter.

Next, we investigated the effects of ethanol pretreatment on heat stress tolerance in tomato seedlings. After ethanol pretreatment for 3 d or 6 d, the seedlings were subjected to heat stress treatment of 50°C for 4 h then grown under normal growth conditions for 7 d. The green leaf areas of seedlings pretreated with ethanol for 3 d were greater than those of seedlings pretreated with water ( Figures 1A, B ). A similar result was observed in the seedlings of ethanol pretreatment for 6 d ( Figures 1C, D ). These results suggested that ethanol pretreatment reduced the leaf growth damage caused by heat stress in tomato seedlings.

Figure 1 Heat tolerance of tomato ‘Micro-Tom’ seedlings treated with water or ethanol. Sixteen-day-old seedlings were pretreated with water or 20 mM ethanol for 3 d or 6 d then subjected to heat stress treatment (50 °C, 4 h). After the heat treatment, the seedlings were grown under normal conditions for 7 d. (A) Appearance of seedlings with 3 d pretreatment. (B) Box plot of green leaf areas of seedlings in (A) . (C) Appearance of seedlings with 6 d pretreatment. (D) Box plot of green leaf areas of seedlings in (C) . (B, D) n = 8. Different letters indicate significant differences at P < 0.05 ( t -test).

3.2 Effects of ethanol pretreatment and heat stress treatment on tomato fruit development

To investigate the effects of ethanol pretreatment and heat stress treatment on tomato fruit development, plants were grown until the mature fruit stage after ethanol pretreatment and heat stress treatment ( Figure 2A ). The appearance of plants after 1 d and 41 d of the heat treatment (seedling stage and flower developmental stage) was also shown in Supplementary Figure S2 . The fruit numbers of the plants treated with ethanol were higher than those of the plants treated with water ( Figure 2B ). The fresh weight per fruit was not different between ethanol- and water-treated plants ( Figure 2C ). These data suggested that ethanol pretreatment might be effective for alleviating heat damage to fruit development.

Figure 2 Effects of heat stress after ethanol treatment on tomato ‘Micro-Tom’ fruit development. Sixteen-day-old seedlings were pretreated with water or 20 mM ethanol for 3 d then subjected to heat stress treatment (50 °C, 2.5 h). After the heat treatment, the seedlings were grown under normal condition for 110 d. (A) Appearance of plants. (B) Box plot of fruit number. (C) Box plot of fruit fresh weight. (B, C) n = 5 to 6. Different letters indicate significant differences at P < 0.05 ( t -test).

3.3 Effects of ethanol pretreatment and heat stress treatment on water use efficiency

WUE is an important parameter that shows a relationship between plant growth and water use. To investigate the effects of ethanol pretreatment and heat stress treatment on WUE, we first estimated transpiration volumes during those periods. The transpiration volume during ethanol pretreatment was lower than that during water pretreatment ( Supplementary Figure S3A ). Next we checked transpiration volumes and leaf areas before heat stress treatment and after 9 d of heat stress treatment. During 9 d after the heat stress treatment, the transpiration volume and leaf area of ethanol-pretreated seedling were greater than those of water-pretreated seedling ( Supplementary Figures S3B, C ). Using these data, we calculated WUE during 9 d after the heat stress treatment by the formula: difference in green leaf area/transpiration volume. The result showed that the WUE of ethanol-pretreated seedling was not different from that of water-pretreated seedling ( Supplementary Figure S3D ). Finally, it was shown that the fresh weight of shoot of ethanol-pretreated seedling was higher than that of water-pretreated seedling ( Supplementary Figure S3E ).

3.4 Effects of ethanol pretreatment and heat stress treatment on plant biomass

Next we investigated the effects of ethanol pretreatment and heat stress treatment on plant biomass. The fresh and dry weights of shoots of seedlings pretreated with water were significantly decreased by heat stress treatment ( Supplementary Figures S4A, C ). On the other hand, the fresh and dry weights of shoots of seedlings pretreated with ethanol were not significantly decreased by the same stress treatment ( Supplementary Figures S4A, C ). These results suggest that ethanol pretreatment alleviated the shoot growth damage. In the case of roots, a similar result was acquired in the samples of dry weight, not in the samples of fresh weight ( Supplementary Figures S4B, D ).

3.5 Effects of ethanol pretreatment on stomatal aperture in tomato

Previous studies showed that ethanol treatment caused stomatal closing in Arabidopsis ( Bashir et al., 2022 ) and cassava ( Vu et al., 2022 ). We checked stomatal apertures in tomato plants treated with ethanol or water. As expected, the stomatal apertures of the seedlings treated with ethanol were smaller than those of the seedlings treated with water ( Supplementary Figure S5 ).

3.6 Temporal and spatial gene expression profiles of ethanol-pretreated and heat stress-treated tomato plants

To elucidate the temporal and spatial gene expression profiles of ethanol-pretreated and heat stress-treated tomato plants, we performed transcriptome analysis using various organs at different developmental stages. First, we performed RNA-seq analysis using seedlings. Figure 3A indicates the diagrams of the sampling time points. Principal component analysis showed that each sample was mostly separated from the others, suggesting different gene expression profiles among these treatments ( Figure 3B ). We then analyzed differentially expressed genes (DEGs) between water- and ethanol-treated samples ( Figure 3 , Supplementary Figure S6 , Supplementary Tables S2–S9 ). For example, in the shoot, 157, 562 and 603 genes were found as up-regulated DEGs in the comparisons E3d vs W3d, E3d_H30m vs W3d_H30m, and E3d_H90m vs W3d_H90m, respectively. In roots, 414, 241, 470 genes were found as up-regulated DEGs in the same comparisons. Venn diagrams for each DEG set showed that some of the DEGs overlapped among E3d vs W3d, E3d_H30m vs W3d_H30m, and E3d_H90m vs W3d_H90m ( Figure 3C ). For example, among the shoot up-regulated DEGs, 63% (99/157 genes) of the DEGs of E3d vs W3d overlapped with the DEGs of E3d_H30m vs W3d_H30m and/or E3d_H90m vs W3d_H90m. We also compared the DEGs between shoot and root, indicating that most DEGs did not overlap in the comparisons ( Figure 3D ). Gene ontology (GO) analysis showed that various GO terms were enriched in the DEGs ( Supplementary Tables S10–S22 ). Figure 3E shows the representative enriched GO terms in the up- and down-regulated DEGs. Stress-related GO terms such as “defense response”, “water deprivation”, “ROS metabolic process”, and “jasmonic acid biosynthesis” were found in the up-regulated DEGs while photosynthesis-related GO terms were included in the down-regulated DEGs.

Figure 3 Transcriptome analysis of seedlings heat stressed for 30 min or 90 min. Fifteen-day-old seedlings were pretreated with water or 20 mM ethanol for 3 d then subjected to heat stress. (A) Diagrams of sampling time points for transcriptome analysis. Stars show the sampling time points with codes to denote the different treatments. (B) Principal component analysis of transcriptome data. (C) Venn diagrams of number of differentially expressed genes (DEGs) in comparisons among treatments E3d vs W3d, E3d_H30m vs W3d_H30m, and E3d_H90m vs W3d_H90m. (D) Venn diagrams of number of DEGs in comparison between shoot and root. (E) Representative GO terms enriched in DEGs. Asterisks show the significance of enrichment (Fisher’s exact test, P < 0.05).

We also performed RNA-seq analysis using samples of mature green fruits (MGFs) and leaves at the developmental stage of MGF after the ethanol pretreatment and heat stress treatment ( Figure 4A ). In the MGF, 191 and 12 genes were identified as up- and down-regulated DEGs, respectively ( Figure 4B , Supplementary Table S8 ). In the leaf, only four and three genes were identified as up- and down-regulated DEGs, respectively ( Figure 4B , Supplementary Table S9 ). For further analysis, we focused on the up-regulated DEGs of MGF. Venn diagrams showed that most of the up-regulated DEGs of MGF did not overlap with the DEGs of shoot and root ( Figure 4C ). The up-regulated DEGs of MGF included the enriched GO terms involved in seed development and seed components such as lipids ( Figure 4D , Supplementary Table S22 ).

Figure 4 Transcriptome analysis of mature green fruit (MGF) and leaf at MGF stage after water or ethanol pretreatment and heat stress treatment. Fifteen-day-old seedlings were pretreated with water or 20 mM ethanol for 3 d and the seedlings were subjected to heat stress for 2.5 h. After the heat treatment, the plants were grown under normal conditions and MGFs were sampled. (A) Diagram of sampling time points for transcriptome analysis. Stars show the sampling time points with codes to denote the different treatments. (B) Volcano plots of transcriptome analysis. Horizontal green lines indicate the threshold value of q-value (q < 0.05). Vertical green lines show the threshold values of up-regulated DEG (log 2 fold change ≥ 1) and down-regulated DEG (log 2 fold change ≤ 1). (C) Venn diagrams of number of DEGs in comparisons as indicated. (D) Representative GO terms enriched in up-regulated DEGs in MGF. Asterisks show the significance of enrichment (Fisher’s exact test, P < 0.05).

To confirm the results of the RNA-seq analysis, we performed RT–qPCR analysis regarding two SlLEAs (Solyc02g085150 and Solyc09g014750) and SlDREB2A (Solyc05g052410). Similar results were acquired in the RT–qPCR analysis ( Supplementary Figure S7 ), which validated the results of the RNA-seq analysis.

3.7 Metabolites that were increased or decreased after ethanol pretreatment and heat stress treatment in tomato seedlings and fruits

To reveal the metabolites that increased or decreased after ethanol pretreatment and heat stress treatment in tomato seedlings and fruits, we analyzed metabolites by gas chromatography–mass spectrometry (GC–MS). Figure 5A shows the time points for this analysis and the codes denoting the different samples. We measured the contents of 81 metabolites (23 amino acids, 9 amines, 18 organic acids, 10 sugars, 3 alcohols, and 18 others) ( Supplementary Tables S23–S29 ). Using these data, we identified metabolites differentially accumulated between water- and ethanol-pretreated samples ( Supplementary Tables S30–S37 ). In the comparisons of shoot (E3d_H150m vs W3d_H150m) and root (E3d_H150m vs W3d_H150m), it was found that 17 and 25 metabolites were differentially accumulated, respectively ( Supplementary Tables S32, S33 ). Clustering analysis showed that some of the ethanol-induced metabolites overlapped between shoot E3d_H150m vs W3d_H150m and root E3d_H150m vs W3d_H150m ( Figure 5B ). They included fructose, sucrose, glucose, fructose-6-phosphate, and glucose-6-phosphate ( Supplementary Tables S32, S33 ). The contents of putrescine in root E3d_H150m and mature red fruit (MRF) E3d_H150m_MRF were also higher after ethanol pretreatment than in the water-pretreated samples ( Supplementary Tables S33, S36 ).

Figure 5 Metabolome analysis. (A) Diagram of sampling time points for metabolome analysis. Stars show the sampling time points with codes to denote the different treatments. (B) Clustering analysis of fold changes of metabolites between water- and ethanol-treated plants. Only significantly different fold change values (q-value < 0.05) were used in this clustering analysis.

We also measured the starch contents in the samples at the MGF stage. The contents in ethanol-pretreated fruit and leaf samples were not significantly different from those in water-pretreated ones ( Supplementary Figure S8 ).

3.8 Enrichment of intrinsically disordered region proteins in up-regulated DEGs

Our previous paper discussed that ethanol treatment might affect the formation of biomolecular condensates driven by liquid–liquid phase separation (LLPS) ( Matsui et al., 2022 ). Because intrinsically disordered region (IDR) proteins have been recognized as an important factor of the LLPS event ( Field et al., 2023 ; Liu et al., 2023 ), we estimated the enrichment of IDR proteins in the up-regulated DEGs identified by the present RNA-seq analysis. While the proportion of IDR proteins in total tomato proteins was 47.3%, significantly higher proportions of IDR proteins were found in the DEGs of root E3d vs W3d (54.1%), shoot E3dH30m vs W3dH30m (57.1%), and shoot E3dH90m vs W3dH90m (60.7%) ( Table 1 ).

Table 1 Enrichment of intrinsically disordered region proteins in up-regulated DEGs.

4 Discussion

The purpose of this paper was to investigate whether ethanol application enhances heat stress tolerance in tomato. As in other plant species reported previously, our results in tomato showed that ethanol pretreatment alleviated heat damage to vegetative growth ( Figure 1 ). In addition, we demonstrated that ethanol pretreatment was also effective for improving reproductive development after heat damage ( Figure 2 ). Although the fresh weight per fruit was not different between ethanol- and water-treated plants, the fruit number per plant was higher in ethanol-treated plants than in water-treated control plants ( Figure 2 ). This suggests that ethanol pretreatment can improve yield of fruits or seeds under heat stress conditions.

Previously, we reported that ethanol pretreatment enhanced heat stress tolerance in Arabidopsis ( Matsui et al., 2022 ). That study showed that ethanol treatment increased the expression level of Binding Protein 3 (BIP3) , a marker gene for endoplasmic reticulum (ER) stress ( Matsui et al., 2022 ). We also observed that unfolded protein response (UPR)-related metabolites such as polyamines accumulated in ethanol-treated Arabidopsis plants ( Matsui et al., 2022 ). These results raised the possibility that ethanol treatment might activate UPR signaling in Arabidopsis. This hypothesis was supported by the results that UPR inducer treatment increased heat stress tolerance while UPR inhibitor treatment decreased heat stress tolerance; furthermore, the reduced heat stress tolerance was found in the mutant bzip60 ( Matsui et al., 2022 ). The protein bZIP60 has been shown to function as an upstream regulator of BIP3 ( Humbert et al., 2012 ; Pastor-Cantizano et al., 2020 ). In the present study, the expression levels of tomato BIP family genes (Solyc01g099660, Solyc01g150132, Solyc03g082920, Solyc06g052050, Solyc08g082820, and Solyc12g055687), bZIP60 (Solyc10g078290), and also bZIP28 (Solyc04g082890), which is another upstream regulator of BIP3 ( Fragkostefanakis et al., 2015 ; Löchli et al., 2022 ), were not different between water- and ethanol-treated samples at seedling stages ( Supplementary Tables S2–S7 ). However, it is interesting to note that the content of the polyamine putrescine was higher in some comparisons between ethanol- and water-treated samples ( Figure 5 ). Although the expression levels of BIP3 , bZIP60 and bZIP28 were not increased by ethanol application, we found that expression levels of several genes encoding molecular chaperones other than BIP family genes were increased in shoot E3H90m vs W3H90m (Solyc09g092260), in root E3 vs W3 (Solyc05g015470, Solyc07g065970, and Solyc08g005300), and in root E3H90m vs W3H90m (Solyc03g115140, Solyc05g050820, and Solyc08g005300) ( Supplementary Tables S3, S6, S7 ). These chaperones might play a role in the UPR machinery of ethanol-treated tomato plants.

Physicochemical properties of ethanol molecules affect liquid–liquid phase separation (LLPS) ( Hansen et al., 2021 ). LLPS has received much attention in biological regulatory processes, not only in yeasts and animals but also in plants ( Londoño Vélez et al., 2022 ; Field et al., 2023 ; Liu et al., 2023 ). In the biological aspects of LLPS, accumulating evidence has demonstrated that intrinsically disordered region (IDR) proteins function as important molecules involved in the formation of biomolecular condensates ( Han et al., 2023 ). For example, the yeast prion protein Sup35 functions in the formation of biomolecular condensates to rescue the translation factor from stress-induced injury ( Franzmann et al., 2018 ). We checked the enrichment of IDR proteins in the up-regulated DEGs identified by the RNA-seq analysis ( Table 1 ). The proportions of IDR proteins in the up-regulated DEGs (root E3d vs W3d, shoot E3dH30m vs W3dH30m, and shoot E3dH90m vs W3dH90m) were significantly higher than the proportion of IDR proteins among proteins as a whole in tomato ( Table 1 ). The observed high proportion of IDR proteins in the up-regulated DEGs suggest that ethanol treatment might induce a cellular state where biomolecular condensates can be easily formed by LLPS. We also found that the GO term “red or far-red light signaling” was enriched in the up-regulated DEGs in shoots ( Figure 3E ). This raises a possibility that phytochrome B regulatory pathways are affected by ethanol application. It is intriguing that phytochrome B functions as one of the thermosensors ( Legris et al., 2016 ; Piskurewicz et al., 2023 ) and is involved in the formation of the biomolecular condensate photobody in the nucleus ( Chen et al., 2022 ; Shi and Zhong, 2023 ). Furthermore, we noticed that the expression levels of some of the late embryogenesis abundant ( LEA) genes were up-regulated by ethanol application. For example, the expression level of Solyc02g085150 in the shoot E3d sample was higher than that in the shoot W3d sample (log 2 fold change = 2.28) ( Supplementary Table S2 ). This expression difference was confirmed by quantitative RT–PCR analysis ( Supplementary Figure S7A ). Our RNA-seq analysis showed that 3, 6, and 3 LEA genes were up-regulated in shoot E3d vs W3d, shoot E3dH30m vs W3dH30m, and shoot E3dH90m vs W3dH90m, respectively ( Supplementary Tables S2, S4, S6 ). LEA proteins function as protective molecules that bind directly to client proteins and prevent aggregation not only under drought stress conditions but also under heat stress conditions ( Dirk et al., 2020 ; Hernández-Sánchez et al., 2022 ). The shrimp LEA protein AfrLEA6 is involved in desiccation tolerance through LLPS ( Belott et al., 2020 ). If LLPS in the ethanol-treated plants is activated, we suggest that the accumulation of LEA proteins by LLPS might be one of the factors that contribute to enhanced stress tolerance. To elucidate the involvement of ethanol-mediated cellular status in LLPS, further analysis is needed. We are investigating whether ethanol application affects the formation of biomolecular condensates by LLPS.

Bashir et al. (2022) showed that, in ethanol-treated Arabidopsis plants, the ethanol incorporated into cells was converted to sugars via the gluconeogenesis pathway. In our RNA-seq analysis, we found that the expression levels of some genes encoding enzymes associated with ethanol metabolism were up-regulated following ethanol application. The expression levels of the genes (Solyc02g084640, Solyc02g086970, and Solyc05g005700) encoding aldehyde dehydrogenase, which converts aldehyde into acetic acid, were increased in the root E3dH90m ( Supplementary Table S7 ). The expression level changes of these genes might reflect the incorporation of the applied ethanol into sugars in the root cells. Because aldehyde molecules are toxic for organisms, the increased expression of genes encoding aldehyde dehydrogenase might be preferred. Our metabolome analysis showed that the contents of sugars, including sucrose, glucose, fructose, glucose-6-phosphate, and fructose-6-phosphate, were increased in ethanol-treated shoots and roots (E3d_H150m) compared with those in water-treated shoots and roots (W3d_H150m) ( Supplementary Tables S32, S33 ). This supports the view that ethanol application activates the gluconeogenesis pathway. The GO terms related to photosynthesis were enriched in the down-regulated DEGs ( Figure 3E ), suggesting that sugar accumulation after ethanol application might cause the down-regulation of photosynthesis-related genes and so save photosynthetic effort.

Trehalose is one of the compatible solutes that contribute to modulating osmotic imbalance and stabilizing macromolecules ( Dabravolski and Isayenkov, 2022 ). Our metabolome analysis showed that the contents of trehalose in root E3d, shoot E3d_H150m and root E3d_H150m were higher than those in the water-treated samples ( Supplementary Tables S31–S33 ). This suggests that ethanol-pretreated tomato plants might also show improved tolerance to drought stress. The notion was supported by our finding that GO terms such as “water deprivation” were enriched in the DEGs ( Figure 3E ).

In the present study, ethanol pretreatment was applied at the seedling stage. Although the number of fruit was increased by the ethanol pretreatment, the fruit qualitative traits were not greatly altered. We found only one metabolite was increased in MRF ( Supplementary Table S36 ). Ethanol treatment at a later developmental stage might alter the dynamics of metabolite accumulation in MRF. Because ethanol pretreatment at the seedling stage increased the sugar contents in seedlings, ethanol treatment at a later developmental stage might cause sugars to accumulate in MRF, giving sweeter fruits. Furthermore, trehalose might also accumulate in the MRF. Because trehalose has therapeutic effects against neurodegenerative diseases in mammals ( Yap et al., 2023 ), trehalose-enriched tomato fruit might prove valuable.

In conclusion, we discovered that ethanol pretreatment alleviated heat-stress-induced damage in tomato, not only during seedling growth but also in fruit development. Transcriptome analysis revealed sets of genes that were differentially expressed in shoots and roots of seedlings and in mature green fruits of ethanol-pretreated plants compared with those in water-treated plants. The sets included genes encoding LEAs and ROS-related enzymes. Metabolome analysis revealed that the contents of some sugars, including trehalose, sucrose and fructose, were increased in the ethanol-pretreated seedlings after heat stress.

From these results, we hypothesize a model for ethanol-induced heat stress tolerance mechanisms in tomato ( Figure 6 ). Ethanol application increases the contents of sugars, as a result of ethanol incorporation and its conversion into sugars via gluconeogenesis activation. Although environmental stress generally inhibits photosynthesis and growth, in the ethanol-pretreated plants the accumulated sugars improve growth under stress conditions, compensating for reduced photosynthesis. Concurrently, ethanol treatment up-regulates stress-related genes encoding LEAs and ROS-related enzymes. LEAs most likely involve the formation of biomolecular condensation driven by LLPS while ROS-related enzymes decrease the content of toxic ROS molecules. These processes occur cooperatively in the ethanol-treated plants and so increase their heat stress tolerance. The knowledge presented here will encourage the development of ethanol-based chemical priming technology that would reduce heat stress damage and enhance fruit quality in crops, especially in the Solanaceae. At present, regarding this technology, there is a gap on how to apply for agriculture. Research practices in field and horticultural facility using the knowledge presented here will be important for the feasibility.

Figure 6 Model for mechanism governing ethanol-mediated heat stress tolerance in tomato.

Data availability statement

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: GEO accession GSE245512.

Author contributions

DT: Data curation, Investigation, Writing – original draft. DQ: Data curation, Investigation, Writing – review & editing. MT: Formal analysis, Investigation, Writing – review & editing. YU: Formal analysis, Writing – review & editing. CU: Formal analysis, Writing – review & editing. AE: Data curation, Writing – review & editing. ST: Data curation, Writing – review & editing. JI: Formal analysis, Writing – review & editing. MKu: Formal analysis, Writing – review & editing. MKo: Formal analysis, Writing – review & editing. KS: Project administration, Supervision, Writing – review & editing. AN: Data curation, Formal Analysis, Writing – review & editing. YN: Resources, Writing – review & editing. NM: Resources, Writing – review & editing. SF: Resources, Writing – review & editing. MS: Project administration, Supervision, Writing – review & editing.

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by grants from RIKEN, Japan (to MS), including the RIKEN-AIST Joint Research Fund (full research), Core Research for Evolutionary Science and Technology (JPMJCR13B4 to MS), and A-STEP (JPMJTM19BS to MS) of the Japan Science and Technology Agency (JST), and Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan (Innovative Areas 18H04791 and 18H04705 to MS).


We thank Chieko Torii, Kayoko Mizunashi and Kyoko Y. Mogami for technical support. We thank Huw Tyson, PhD, from Edanz ( ) for editing a draft of this manuscript.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.

Publisher’s note

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Supplementary material

The Supplementary Material for this article can be found online at:


DREB2A, dehydration responsive element binding 2A protein; LEA, late embryogenesis abundant; BIP3, binding protein 3; bZIP28, basic leucine zipper 28; bZIP60, basic leucine zipper 60.

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Keywords: ethanol, heat stress, chemical priming, micro-tom, transcriptome, metabolome

Citation: Todaka D, Quynh DTN, Tanaka M, Utsumi Y, Utsumi C, Ezoe A, Takahashi S, Ishida J, Kusano M, Kobayashi M, Saito K, Nagano AJ, Nakano Y, Mitsuda N, Fujiwara S and Seki M (2024) Application of ethanol alleviates heat damage to leaf growth and yield in tomato. Front. Plant Sci. 15:1325365. doi: 10.3389/fpls.2024.1325365

Received: 21 October 2023; Accepted: 18 January 2024; Published: 19 February 2024.

Reviewed by:

Copyright © 2024 Todaka, Quynh, Tanaka, Utsumi, Utsumi, Ezoe, Takahashi, Ishida, Kusano, Kobayashi, Saito, Nagano, Nakano, Mitsuda, Fujiwara and Seki. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Motoaki Seki, [email protected]

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

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portrait of Graeme Berlyn in 2023

In Memoriam: Graeme Berlyn, E. H. Harriman Professor of Forest Management and Physiology of Trees

Graeme P. Berlyn, a world-renowned expert on the anatomy and physiology of plants and trees who taught at the Yale School of the Environment (YSE) for more than 60 years, died February 16 in Hamden, Connecticut. He was 90.

Berlyn’s breadth of research included wood anatomy, plant embryology, tissue culture, biotechnology, and the morphology and physiology of trees and forests in relation to environmental stress. He published more than 166 journal articles and his book, “Botanical Microtechnique and Cytochemistry,” has more than 2,200 citations. He was an expert on histology and electron microscopy and served as the only plant scientist on the Biological Stain Commission, the international organization that sets the guidelines for the acceptable biotechnique of staining and preparing histological samples, primarily in medicine.

After working for the U.S. Forest Service in Oregon and Washington, Berlyn came to YSE in July, 1960 at the age of 26. His early work at YSE focused on wood science and cell development, specifically on cottonwood.

Graeme Berlyn conducting field research with instrumentation on a truck tailgate

Through the decades, Berlyn, E. H. Harriman Professor of Forest Management and Physiology of Trees, became a beloved presence at Greeley Memorial Lab where he would host weekend lunches in the kitchen with his research students, serving meals he cooked and nutrition drinks he had created, often with his dogs by his side. He enjoyed working out with weights in the basement in what fondly became known as the “Heavy Metals  Uptake Lab” to the tunes of Texas swing. Berlyn liked to jog, even before that became popular, was an avid hiker, and also pursued martial arts including Taekwondo.

While at YSE, Berlyn broadened his research focus on wood cellular structure, examining the nuclear effects of radiation on plants; the adaptation of spruce fir to acid rain across elevation gradients; and  leaf morphology and physiology responses to light. One of his most cited papers was on chlorophyll fluorescence. In the 1990s, he pioneered the development of non-hormonal plant biostiumulants and created a line of plant food called “Roots” that helped fund his subsequent research.

Berlyn was involved in the formation of the Tropical Resources Institute (TRI) and participated in a School trip to Jamaica and TRI's first formal field trip to Puerto Rico in 1984, as well as subsequent trips to Venezuela, Costa Rica, Japan, and British Columbia. He also worked in the mountains of British Columbia and the northeastern U.S., collecting plant samples at different gradients.

In 2014 Berlyn worked on developing green wall technology that used recirculated water as an alternative to cooling towers. In 2021, he won the Audience Choice Award at Startup Yale with Kevin Gallagher ’20 YC for a nonfertilizer biostimulant that helps farmers grow more crops with less land.  His recent research included collaboration with colleagues on blue carbon involving sea grass.

At the heart of all his work was his commitment to his students, said Mark Ashton , senior associate dean of The Forest School at YSE and Morris K. Jesup Professor of Silviculture and Forest Ecology. Ashton first met Berlyn in the 1980s while he was getting his master’s and doctorate at YSE and Berlyn became his mentor.

His students were devoted to him because he was devoted to them.”

Berlyn, who liked to dress in black, could seem intimidating and gruff at first, but he was the opposite, Ashton said.

“He was an absolute softy. If you were a serious student and he saw you working hard, he offered lifetime mentorship. He was an extremely giving person,” Ashton said. “His students were devoted to him because he was devoted to them.”

When one of his students became ill with cancer, Berlyn, who was director of graduate studies at YSE at the time, stayed with him in the hospital until he died.

“The saddest thing for me was losing Anders Claeson, a student here who wanted to do doctoral work on Caribbean Pine in Fiji. It’s painful losing someone so young,” Berlyn recalled in an interview with the alumni office about his time at YSE.

Over the years, Berlyn took great pride in the accomplishments of his former students.

“That’s probably the greatest part of the job — the students we’ve had here,” Berlyn said. “I’ve mentored a number of PhD students … a number of them went on to become professors at various universities and so that’s a very satisfying part of being a professor, that your students make a mark for themselves. And all of them have in one way or another.”

Dean Indy Burke noted Graeme’s enthusiastic mentoring of alumni.

“Our alumni feel a deep sense of connection to Graeme, who came to every reunion to catch up with his students and friends, and they have remained in touch through the years and decades. Graeme graced us all with his sharp intellect, wry grin, and sense of humor.  He remained deeply committed to diversity, equity, and inclusion throughout his entire career, helping us advance our efforts in this important area especially over the last decade. We will miss him deeply,” she said.

When he arrived as an assistant professor at YSE, Craig Brodersen said Berlyn was generous in sharing his knowledge of the School.

“Graeme had an incredible wealth of knowledge not only about plant anatomy, development, and physiology, but also about the history of our School. That kind of institutional knowledge, some of it now passed on to me, has been extremely helpful in better understanding YSE’s past and current role both here at Yale and more broadly,” said Brodersen, professor of  plant physiological ecology. “He was a kind, generous person and I learned a lot from him over the past 10 years working with him. I feel deeply honored to be carrying on the tradition of teaching and research related to plant anatomy and physiology that he helped sustain here at YSE.”

YSE students and alumni recalled Graeme’s openness, cultural sensitivity, and ability to inspire scientific curiosity.

Andrew Richardson ’98 MF ’03 PhD, professor at the School of Informatics, Computing, and Cyber Systems at Northern Arizona University, said Berlyn was more than a role model to him, showing him how to persevere through tough times.

“I showed up at Yale in the fall of 1996, an enthusiastic but naive first-year MF student, knowing little about forest ecology, silviculture, or plant physiology (my undergraduate degree had been in economics). Nevertheless, Graeme took me on as a research assistant, and over the next seven years, he trained me, mentored me, and supported me in ways that enabled me to grow as a scientist and scholar, and learn from my mistakes,” Richardson said. “This was a difficult time for Graeme. He had been diagnosed with cancer, and though he must have suffered enormously from the chemotherapy treatments, he still made it into the lab virtually every day.”

Graeme graced us all with his sharp intellect, wry grin, and sense of humor.  He remained deeply committed to diversity, equity, and inclusion throughout his entire career, helping us advance our efforts in this important area especially over the last decade. We will miss him deeply.”

Helen Poulos ’07 PhD, a forest and fire ecologist and associate professor of earth and environmental sciences at Wesleyan who co-authored 10 peer-reviewed studies with Berlyn, remembered her lunchroom conversations with him at Greeley Lab while she was a doctoral student.

“It was through those lunchroom conversations that I started working with Graeme and decided to take his classes. He was just available to students in a way that made it easy to talk with him, ask questions, think about big ideas, design experiments, and do research,” she said. “Graeme's fascination with the dynamic lives of trees was infectious. He taught me, and thousands of other Yalies how plants survive, grow, and reproduce through the lens of plant ecophysiology. I will be forever grateful for my time with him.”

Muhammad Sohail Yousaf, a postdoctoral fellow at the Greeley Lab who had been working closely with Berlyn, noted his scientific expertise.

“What stood out to me the most about Graeme was his unwavering commitment to excellence. Whether it was in the classroom, in his research, or in his interactions with others, he always strived for the highest standards and encouraged those around him to do the same. Graeme's contributions to the field were significant and far-reaching. His research pushed the boundaries of our understanding and opened up new avenues for exploration. His dedication to advancing the field will continue to impact generations of scholars,” he said.

Kaisone Phengsopha ’05 MEM, acting dean of the faculty of environmental science at the National University of Laos, said Berlyn made every student at YSE feel welcomed.

“Professor Berlyn was not only an exemplary scholar but also a guiding light for many of us. His dedication to nurturing young scientists from diverse backgrounds was not limited to students from the U.S. He left an indelible mark on the academic journeys and personal growth of foreign students including myself. During my student days at Yale, I am particularly grateful for his showing me the concern on and interests in the history and tradition of my country, Korea. He embodied the true spirit of Yale's academic excellence and compassion, inspiring not just a passion for learning but a deep commitment to making a meaningful impact in the world,” Phengsopha said.

Berlyn is survived by his wife Mary Berlyn  ’66 PhD,  and two children, Dina and John. YSE is planning a recognition ceremony  in coordination with Berlyn’s family that will be announced at a later date. 

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Climate Change, Population Growth, and Population Pressure

We develop a novel method for assessing the effect of constraints imposed by spatially-fixed natural resources on aggregate economic output. We apply it to estimate and compare the projected effects of climate change and population growth over the course of the 21st century, by country and globally. We find that standard population growth projections imply larger reductions in income than even the most extreme widely-adopted climate change scenario (RCP8.5). Climate and population impacts are correlated across countries: climate change and population growth will have their most damaging effects in similar places. Relative to previous work on macro climate impacts, our approach has the advantages of being disciplined by a simple macro growth model that allows for adaptation and of assessing impacts via a large set of climate moments, not just annual average temperature and precipitation. Further, our estimated effects of climate are by construction independent of country-level factors such as institutions.

We are grateful to Lint Barrage, Greg Casey, Maureen Cropper, Eric Galbraith, and Zeina Hasna for helpful advice; to Lucy Li, Frankie Fan, William Yang, and Raymond Yeo for research assistance; to David Anthoff, Brian Prest, and Lisa Rennels for access to data and code; and to seminar audiences at the Bank of Italy, University of Bologna, Université Catholique de Louvain, University of Chicago, University of Chile, University of Connecticut, ETH Zurich, IIASA, Korea University, Lahore School of Economics, University of Manchester, NBER Summer Institute, NYU Abu Dhabi, Osaka University, Oxford University, RIDGE forum on Sustainable Growth, Schumpeter Seminar (Humboldt University), Sungkyunkwan University, University of Tokyo, and the World Bank for useful feedback. Research was supported by the Population Studies and Training Center at Brown University through the generosity of the Eunice Kennedy Shriver National Institute of Child Health and Human Development (P2C HD041020 and T32 HD007338).}} The views expressed herein are those of the authors and do not necessarily reflect the views of the National Bureau of Economic Research.

In the past three years I have received significant research funding from the World Bank, the International Growth Centre and the U.S. Department of Transportation.


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The influences of four types of soil on the growth, physiological and biochemical characteristics of Lycoris aurea (L’ Her.) Herb

Miaohua quan.

1 College of Biological and Food Engineering, Huaihua University, Huaihua, Hunan 418008, P. R. China

2 Key Laboratory of Hunan Province for Study and Utilization of Ethnic Medicinal Plant Resources, Huaihua, Hunan 418008, P. R. China

3 Key Laboratory of Hunan Higher Education for Hunan-western Medicinal Plant and Ethnobotany, Huaihua, Hunan 418008, P. R. China

Associated Data

Based on the characteristics of Lycoris aurea (L. aurea ) natural distribution and local soil types, we selected four representative types of soil, including humus soil, sandy soil, garden soil and yellow-brown soil, for conducting the cultivation experiments to investigate key soil factors influencing its growth and development and to select the soil types suitable for cultivating it. We found that there existed significant differences in the contents of mineral elements and the activities of soil enzymes (urease, phosphatase, sucrase and catalase) etc. Among which, the contents of organic matters, alkali-hydrolysable nitrogen, Ca and Mg as well as the activities of soil enzymes in humus soil were the highest ones. In yellow-brown soil, except for Fe, the values of all the other items were the lowest ones. Net photosynthetic rate ( P n ), biomass and lycorine content in humus soil were all the highest ones, which were increased by 31.02, 69.39 and 55.79%, respectively, as compared to those of yellow-brown soil. Stepwise multiple regression analysis and path analysis indicated that alkali-hydrolysable nitrogen, and Ca etc. were key soil factors influencing P n , biomass and lycorine content of L. aurea . Thus, humus soil can be used as medium suitable for artificial cultivation of L. aurea .

Lycoris aurea (L’ Her.) Herb ( L. aurea ), also known as Golen Magic Lily , is a perennial herbaceous plant belonging to the genus Lycoris . It is a traditional Chinese medicinal herb plant 1 . Its bulb is rich in more than 10 types of alkaloids, including lycorine, galanthamine and lycoramine etc. and can be used to treat several important diseases such as poliomyelitis sequel, Alzheimer’s disease, and myasthenia Gravis etc. It also possesses certain anti-cancer effects and has been used in treating cancer. Thus, it has important medicinal value 2 . Lycorine belongs to pyrrolo-phenanthridine alkaloid within the class of isoquinoline alkaloids and is one of the major components of the anti-cancer alkaloids present in the plants in the family Amaryllidaceae 3 , 4 . Moreover, L. aurea is also a good groundcover and ornamental flower plant. Its bulb is also rich in starch and galanthus nivalis agglutinin. Thus, it is valuable to be widely applied in many fields, including landscape garden, industry and agriculture 5 . Its bulb contains many types of abundant components such as alkaloids and has relatively higher ornamental value. Thus, there is increasing market demand on L. aurea . However, in the recent years, the deterioration of the ecological environment and the over-artificial digging had led to the shortage of the resources of wild L. aurea . Thus, to initiate the artificial cultivation of L. aurea is of theoretical importance and practical significance for protection and proper utilization of the rare resource of wild L. aurea .

The quality of herb medicines is the comprehensive indicator reflecting certain cultivation technologies and ecological conditions under which the medicinal plants grow. Among which, soil serves as an essential medium for supporting plant growth and development, and thus, it has important influences on the growth, development and the medicinal quality of herb plants 6 . The nutritional elements (e.g. N, P, K, Ca, and Mg etc.) of soil are required for the growth of medicinal plants. These elements are not only the important sources of materials for building up the structures of plant tissues, but also are actively involved in the metabolic activities within plants 7 . For instance, Barlóg 8 reported that magnesium and nitrogenous fertilizers were favorable for the growth, the biosynthesis and accumulation of alkaloids in Lupinus angustifolius . Ca 2+ plays important roles in sequestration and signaling in regulating the activities of chloroplasts 9 , 10 . Plants require K + for important intracellular physiological functions, including photosynthesis and nutrient transport 11 . Soil enzymes are one type of the most important biological components of the soil ecosystem. They play an important role in organic matter decomposition and nutrient cycling 12 . For instance, the hydroxylases (e.g. urease and sucrase etc.) can hydrolyze the macromolecules, such as proteins and polysaccharides, to form the simpler and smaller molecules that are easily absorbed by plants and to accelerate the nitrogen cycle and carbon cycle within the soil ecosystem. The activities of soil enzymes are closely related to soil physicochemical properties, soil types, and fertilizer application, cultivation and other agricultural measures 13 , 14 . Alkaloids are an important class of plant secondary metabolites and the result of the interactions between plants and their environments (both biotic and abiotic) during the long-term evolution process 15 , 16 . Different types of soil possess different textures and physiochemical properties while the demands of different types of medicinal herb plants for suitable soil conditions are quite different. Thus, the types of soil for cultivation of medicinal herb plants should be selected according to the particular physiological requirements of the particular plants 6 , 17 . Currently, most of the studies on L. aurea have mainly focused on the such aspects as biological evolution 18 , 19 , chemical compositions 20 , 21 , 22 , physiology and biochemistry 23 , 24 , 25 , pharmacology and pharmacodynamics 2 , 26 , 27 . In term of cultivation, Zeng et al . 28 reported that L. aurea preferred the environments of shading, humidity, pleasantly cool, ventilation and penetrating light and had no strict requirement for soil type, but it grew better in sandy loam and calcific soil etc. that were fertile, porous, and rich in organic matter. However, the studies on the effects of soil conditions on the growth and development of L. aurea and the accumulation of the medicinal components have been barely available. Thus, it is necessary to select suitable soil conditions for artificial cultivation of L. aurea . In this study, based on the characteristics of its natural distribution patterns, we selected four representative types of soil with different textures and physiochemical properties for conducting the controlled experiments on the cultivation of L. aurea, aiming to study the correlations of the key soil factors with its growth, development and accumulation of medicinal component for providing the experimental basis for artificial cultivation of L. aurea.

Comparison in physicochemical properties among different types of cultivation soil

As shown in Table 1 , there were significant differences in pH value, the contents of soil moisture, organic matter, alkali-hydrolysable nitrogen, rapidly available phosphorus, rapidly available kalium, Ca and Mg etc. in different types of soil. Among which, the contents of organic matter, alkali-hydrolysable nitrogen, Ca and Mg were the richest ones in humus soil, which were 22.64, 7.99, 11.66 and 5.88 times those of yellow-brown soil, the poorest ones. The Fe content in yellow-brown soil was the highest one. The contents of soil moisture, rapidly available phosphorus, rapidly available kalium, Zn, Mn and Cu in garden soil were higher but its Mo content was extremely low. The Mo content in sandy soil was the highest one while the contents of the remaining compositions were between the other types of soil. The humus soil, sandy soil and garden soil were all alkalescent while yellow-brown soil was acidic.

Data followed by different letters within the same line are significantly different (p < 0.05). Mean ±  SM represents their standards of error, n = 5. DW represents dry weight.

Comparison and analysis on major agronomic trials of L. aurea among different types of cultivation soil

Different types of cultivation soil had different impacts on the major agronomic trials of L. aurea ( Table 2 ). The biomass performances, the bulb diameter, floral axis height, leaf length and leaf width were all the highest ones in humus soil, which were increased by 69.39, 14.50, 11.74, 15.72 and 8.06%, respectively, as compared to those in yellow-brown soil in which their performances were poorest. The differences in these parameters between two types of soil were statistically significant (P < 0.05). Their performances in sandy soil and garden soil were between those of the humus soil and yellow-brown soil.

Data followed by different letters within the same column are significantly different (p < 0.05). Mean ±  SM represents their standards of error, n = 15. DW represents dry weight.

Comparison and analysis on photosynthetic parameters of L. aurea among different types of cultivation soil

Different types of cultivation soil had different effects on photosynthetic parameters of L. aurea ( Table 3 ). Among which, the net photosynthetic rate ( P n ), chlorophyll content, transpiration rate ( T r ), intercellular CO 2 concentration ( C i ) and stomatal conductance ( G s ) were all the highest ones in humus soil. Except for the lowest T r value in sandy soil, the performances of all the remaining parameters in yellow-brown soil were the poorest ones. Compared to those in yellow-brown soil, P n and chlorophyll content were significantly increased by 31.02 and 25.32%, respectively (P < 0.01).

Data followed by different letters within the same column are significantly different ( P  < 0.05). Mean ±  SM represents their standards of error, n = 15. FW represents fresh weight.

Comparison and analysis on the activities of soil enzymes among different types of cultivation soil

As shown in Table 4 , there existed differences, to certain extend, in the activities of soil enzymes of L. aurea among four types of cultivation soil. Among which, the activities of soil enzymes in humus soil were the highest ones whereas those in yellow-brown soil were the lowest ones. Compared to those in yellow-brown soil, the activities of urease, sucrase, phosphatase and catalase were significantly increased by 9.63, 1.64, 4.03 and 1.95 times, respectively (P < 0.01). Among the soil enzymes tested, the activities of both urease and sucrase in four types of soil were also higher whereas the activity of catalase was the lowest one.

Data followed by different letters within the same column are significantly different (p < 0.05). Mean ±  SM represents their standards of error, n = 5. DW represents dry weight.

Comparison and analysis on the lycorine content of L. aurea among different types of cultivation soil

The chromatogram of the bulb sample of L. aurea in cultivation soil were shown in Fig. 1b . The lycorine content of L. aurea in four types of cultivation soil was in the order from high to low as follows: humus soil (1.48 mg g −1 DW) >sandy soil (1.35 mg g −1 DW) >garden soil (1.27 mg g −1 DW) >yellow-brown soil (0.95 mg g −1 DW). Among which, the lycorine content of L. aurea in humus soil was significantly increased by 55.79%, as compared to that in yellow-brown soil (P < 0.01).

An external file that holds a picture, illustration, etc.
Object name is srep43284-f1.jpg

*The objective peak of lycorine.

Analysis on key soil factors significantly influencing the medicinal quality of L. aurea

Stepwide multiple regression analysis on soil factors significantly influencing the medicinal quality of l. aurea.

The measured values of the soil nutrients and mineral elements were taken as the soil factor group while the measured values of P n , biomass and lycorine content were taken as the L. aurea medicinal quality group. The soil factors, including pH ( X 1 ), soil moisture ( X 2 ), organic matter ( X 3 ), alkali-hydrolysable nitrogen ( X 4 ), rapidly available phosphorus ( X 5 ), rapidly available kalium ( X 6 ), Ca ( X 7 ), Mn ( X 8 ), Fe ( X 9 ), Na ( X 10 ), Zn ( X 11 ), Cu ( X 12 ), Mn ( X 13 ), and Mo ( X 14 ), were taken as the independent variables, i.e. soil factor group while the leaf P n ( Y 1 ), biomass ( Y 2 ) and lycorine content ( Y 3 ) of L. aurea were taken as the dependent variables, i.e. medicinal quality group. The soil factors were selected with stepwide multiple regression method. The stepwide multiple regression equations between the L. aurea medicinal quality and significant soil factors were formulated ( Table 5 ). As shown in Table 5 , the significant soil factors influencing leaf P n were alkali-hydrolysable nitrogen ( X 4 ) and Mo( X 14 ) while the significant soil factor influencing the biomass was alkali-hydrolysable nitrogen ( X 4 ); the significant soil factors influencing the lycorine content were alkali-hydrolysable nitrogen ( X 4 ), Ca ( X 7 ) and soil moisture ( X 2 ). Thus, the significant soil factors influencing the medicinal quality of L. aurea are alkali-hydrolysable nitrogen, Ca, Mo and soil moisture.

Path analysis on the key soil factors significantly influencing P n , biomass and lycorine content of L. aurea

In order to further confirm the key soil factors significantly influencing P n , biomass and lycorine content of L. aurea, SPSS statistics analysis was conducted on the significant soil factors and the results were presented in Table 6 . As shown in Table 6 , the effects of alkali-hydrolysable nitrogen on P n , biomass and lycorine content of L. aurea were the greatest ones with determination coefficients of 0.927, 0.976 and 0.833, respectively, indicating that among these factors, alkali-hydrolysable nitrogen is the most significant one; The determination coefficient for the effect of Ca on lycorine content of L. aurea was 0.666, which was ranked the second place among the factors tested, indicating that Ca has important effect on the accumulation of lycorine in L. aurea . Mo had little direct effect on leaf P n of L. aurea (R 2  = 0.015); Soil moisture had negative effect on the lycorine content as its determination coefficient was negative, indicating that soil moisture is a limiting factor. Thus, the key soil factors significantly influencing P n , biomass and lycorine content of L. aurea were alkaline-hydrolysable nitrogen and Ca etc.

R 2 represents coefficient of determination.

L. aurea has been used as a traditional Chinese medicinal herb plant to treat several important diseases. However, the increasing demand on L. aurea is contradictory to the limited supply source of wild L. aurea due to the deterioration of its inhabitant environment and over-artificial digging. One of the effective ways to resolve this contradiction is to artificially cultivate it in large-scale. Selection of appropriate types of soil for artificial cultivation of L. aurea is an essential step toward this solution. In the present study, we selected four representative types of soil, i.e. humus soil, sandy soil, garden soil and yellow-brown soil, to investigate their effects on the growth, development and accumulation of alkaloids of L. aurea . We determined that humus soil could be the suitable soil type for artificial cultivation of L. aurea, as supported by several lines of evidence as follows: (a) Humus soil contained the most abundant organic matter, alkali-hydrolysable nitrogen, Ca and Mg; (b) Humus soil displayed the best performances in several important agronomic trials, including biomass, the bulb diameter, floral axis height, leaf length and leaf width; (c) Humus soil contained the highest activities of soil enzymes including urease, sucrase, phosphatase and catalase; and (d) L. aurea grown in humus soil contained the highest content of lycorine, an important alkaloid. Furthermore, we also found that the key soil factors significantly influencing P n , biomass and lycorine content of L. aurea were alkali-hydrolysable nitrogen and Ca etc.

Different types of soil have quite different physicochemical and biological properties, which have substantial effects on the growth, development and the active constituents of medicinal plants 29 . Thus, different plants have different demands for appropriate type(s) of soil. For instance, Liu et al . 6 reported that the types and texture of soil were closely related to the growth and development of medicinal plants and that loam soil was the relatively ideal type of soil for the cultivation of root/stem-types of medicinal plants. The results obtained from this study have indicated that the humus soil displays the best comprehensive performances in both agronomic trials and physiological and biochemical characteristics including P n , biomass and lycorine content of L. aurea grown among four different types of soil tested, followed by those of sandy soil, garden soil, and yellow-brown soil in the order from high to low. The differences in comprehensive performances are partially due to the significant differences in texture, pH value and organic matter etc. among the types of soil tested. In this study, measurement of the general physicochemical properties of cultivation soils revealed that humus soil was rich in organic matter content with its looser texture and better permeability. Humus soil, sandy soil and garden soil were all alkalescent while yellow-brown soil was acidic. The correlation analysis revealed that the soil pH value displayed a positive correlation with the lycorine content of L. aurea ( Supplementary Information ), indicating that the alkalescent soil is favorable for the accumulation of lycorine of L. aurea . This result was consistent with that obtained by Chao et al . 30 , who reported that the alkaline soil in North China was favorable for the accumulation of alkaloids while the acidic soil and yellow-brown soil in South China were unfavorable for the accumulation of alkaloids. Furthermore, path analysis indicated that value for the direct effect of soil moisture on the lycorine content was negative, implying that high soil moisture content may be unfavorable for the accumulation of alkaloids such as lycorine in L. aurea . This result was consistent with those obtained by El-Shazly et al . 16 and Bustamante et al . 31 , who reported that drought environment could enhance the biosynthesis of plant alkaloids. The rich organic matter that was constantly decomposed in humus soil can provide the stable supply of nitrogen nutrients etc. for the growth of plants. The physicochemical properties of humus soil, i.e. rich organic matter, alkalescent pH value, the looser texture and thus, lower soil moisture, are favorable for the growth, biosynthesis and accumulation of alkaloids such as lycorine of L. aurea .

Deficiency or shortage of any of the nutritional elements (e.g. N, P, K, Ca, and Mg etc.) will certainly affect the normal growth and development as well as the internal and external qualities of plants 7 . Nitrogen is the most important element among all the nutritional elements required by plants 32 . For instance, the biosynthetic processes of alkaloids require nitrogen involvement. The increased, adequate or surplus nitrogen source was found to be favorable for the biosynthesis of alkaloids in Larkspur 33 . The present study indicated that the contents of alkaline-hydrolysable nitrogen and Ca in humus soil were higher than those in the poorest yellow-brown soil. Its biomass and the lycorine content were increased substantially. Stepwide multiple regression analysis and path analysis indicated that alkaline-hydrolysable nitrogen was the most important soil factor, and Ca is the secondary factor, implying that the higher contents of alkaline-hydrolysable nitrogen and Ca in humus soil are favorable not only for the growth and development of L. aurea but also for the accumulation of alkaloids including lycorine. These results also further confirm that nitrogen nutrient and Ca are the important environment factors stimulating plant growth and the biosynthesis of alkaloids. NO 3 -N and NH 4 -N are two major forms of nitrogen nutrients that are absorbed and utilized by plants. The effectiveness of these two forms of nitrogen element on the growth and development of plants are dependent on the types of plants, the concentrations of NO 3 -N and NH 4 -N and their ratio. The absorption, transport and assimilation during the metabolism processes and the effects on the growth, development and physiological processes are significantly different 34 . During the cultivation of crops, nitrogen nutrient and water supply are two very important controlling factors. Thus, how to maximize the effects of nitrogen nutrients, water and Ca 2+ on stimulation of the growth, development, and the accumulation of alkaloids such as lycorine of L. aurea and the underlying regulatory mechanisms remain to be further investigated.

The microorganisms inhabiting in soil (e.g. bacteria and fungi etc.) play extremely important roles in the formation of soil fertility and the inter-conversion of plant nutrients and also affect the permeability of root cells and root metabolism. They can modify the root secretion and change the rhizosphere nutrients 35 , 36 . In the present study, we found that among four types of soil tested, there existed significant differences in the activities of soil enzymes, including urease and sucrase. Among four types of soil, the humus soil was rich in nutrients, such as organic matter, The activities of its soil enzymes were also higher. But in the poorest yellow-brown soil, the mean activities of soil enzymes were lower. The higher activities of these soil enzymes in the humus soil may be mainly attributed to the higher abundance and activities of soil microorganisms, likely due to the favorable soil conditions for their growth. The high activities of these soil enzymes and active soil microorganisms can continuously drive the degradation and mineralization of soil organic matter and provide the stable supply of nitrogen nutrients etc. for the growth of plants and thus, they are favorable for the growth, development and formation and accumulation of alkaloids, including lycorine of medicinal plants.

In this study, we found that among four representative types of soil tested, the humus soil displayed the best comprehensive performances in terms of the agronomic, physiological and biochemical characteristics including P n , biomass and lycorine content of L. aurea , followed by those of sandy soil, garden soil, and yellow-brown soil in the order from high to low. This humus soil contained higher levels of organic matter, the activities of soil enzymes and mineral elements such as alkali-hydrolysable nitrogen, rapidly available phosphorus, and Ca etc. Its texture was looser and its permeability was quite good. Thus, this type of humus soil was suitable for artificial cultivation of L. aurea . Stepwise multiple regression analysis and path analysis indicated that the key soil factors significantly influencing P n , biomass and lycorine content of L. aurea were alkaline-hydrolysable nitrogen and Ca etc. Soil moisture was a limiting factor, implying that high soil moisture content may be unfavorable for the accumulation of lycorine of L. aurea . Our findings provide not only the guidance for conducting artificial cultivation of L.aurea, but also the methods for accumulation of alkaloids including lycorine of medicinal plants.

Materials and Methods

Materials and cultivation plots.

The material of Lycoris aurea (L’Her.) Herb is an acclimated cultivar original from Huaihau, Hunan Province, China. Given that different medicinal plants have different requirements for soil types suitable for their growth and development, in this study, based on the characteristics of the natural distribution of L. aurea , we selected four representative soil types with quite different textures and physicochemical properties, i.e. humus soil (looser texture and rich in nutrition), sandy soil (loose texture), garden soil (moderate texture) and yellow-brown soil (dense texture). These four types of soil were collected from the original ecological environment in August 2012 and placed on the same experimental field under the same climate conditions for artificial cultivation of L. aurea . This experiment was conducted in Botanical Garden of Huaihua University, Hunan, China. The coordinates of geographical location are 110°01’ E, 27°35’ N, and the level above sea is 267 m. The climate in this location belongs to subtropical humid monsoon. The mean annual atmosphere temperature was 16.9 °C and the mean annual rainfall was 1358.6 mm. A number of bulbs with uniform size were selected and cultivated in the spacing (20 × 20 cm) in the experimental plots. The area of the plot was 1 m 2 . Each experiment was repeated three times. All the other conditions, such as water and light, were the same. The plots were managed with conventional management. The experimental period was from August 2012 to December 2015. This study aimed to investigate the effects of different soil types on the growth, development and accumulation of alkaloids of L. aurea for finding out the appropriate soil type(s) and for providing the reference basis for artificial culture of L. aurea.

Experimental Methods

Measurement of the general physicochemical properties of cultivation soil, soil sampling and measurement of the contents of elements.

The soil samples (0–20 cm depth) were collected from the experimental plots in December 2014. The samples were air-dried at room temperature. After passed through a 2 mm sieve, the soil samples were used for analysis. The contents of elements such as Ca, Mg, Fe and Mn etc. in the samples were determined with Inductively Coupled Plasma-Mass Spectrometry (Agilent7700, USA) in Hunan Food Test and Analysis Center, according to Agricultural Industry Standards or National Quality Standards NY/T 87–1988 and NY/T 296–1995 etc 37 .

Measurement of other factors of the soil samples

The contents of alkali-hydrolysable nitrogen, rapidly available phosphorus, rapidly available kalium were determined with diffusion method, NaHCO 3 extraction-Mo-Sb colorimetric method, and NH 4 OAc extraction-flame spectrophotometry, respectively. The organic matters were determined with potassium dichromate oxidation heating method. The soil water content was measured with oven-drying methd 38 . The pH value was determined by using of PHS-3C precision acidity meter.

Measurement of major agronomic trails

Because L. aurea has the following characteristics: its flowers and leaves do not appear at the same time and it has summer dormancy. Its flowers blossom out in August, its leaf development starts in September and its vigorous growth stage is in December. Thus, the measurements of its agronomic trails in different types of cultivation soil were conducted in two stages. Its floral axis height was measured in August 2014 while its morphological parameters, including leaf length, leaf width and the bulb size were measured in December of the same year. The entire plants, including roots, leaves and bulb, were collected and dried by baking in oven to the constant weight and its biomass was weighted. The bulb samples were ground into powder with grinder (60 meshes) and stored under dry condition for subsequent analysis. Five healthy and strong plants were randomly selected from each sampling site and used as the measured subjects. Three repeat experiments were set.

Measurement of photosynthetic characteristics

Photosynthetic parameters, such as leaf P n , T r , G s , and C i, and other physiological factors were measured by using of Li- 6400 portable photosynthesis measurement system with a red-blue light source ( Li-cor , USA) under saturating light of 1 000 μmol m −2 s −1 . The net photosynthetic rates were measured at least 30 min after the attainment of the temperature 39 . Given that an “afternoon relaxation of photosynthesis” phenomenon exists in L. aurea , measurement of photosynthesis was conducted in morning time. The same positions of the leaves of five randomly selected L. aurea were used to measure P n during 9:00–11:00 am in December 2014 when the plant was in nutrition period 24 . Immediately after that, the corresponding leaves were collected and extracted in 95% ethanol and measured by spectrophotometric method (DU-800 spectrophotometer, Beckman Coulter, Inc.) at the wavelengths 665 and 649 nm. Contents of chlorophyll a and b were calculated by using the method of Lichtenthaler 40 .

Assays of activities of soil enzymes

In the middle 10 days of each month from January to December 2013, the soil samples at 2 cm below the surface soil nearby the root system of L.aurea were collected from various sampling sites. The enzymatic activities in these soil samples were assayed with the method reported by Guan et al . 41 as follows: Urease activity was assayed with indophenol blue colorimetric method and expressed as the amount (in mg) of NH 3 -N/g of dried soil produced within 24 h incubation at 37 °C. Sucrase activity was assayed with 3,5-dinitrosalicylic acid colorimetry and expressed as amount (in mg) of glucose produced within 24 h incubation at 37 °C. Phosphotase activity was assayed with alkaline phosphatase colorimetric method and expressed as the amount (in mg) of phenol produced/g of dried soil within 24 h incubation at 37 °C. Catalase activity was assayed with potassium permanganate titration method and expressed as the volume (in mL) of consumption of 0.1 N KMnO 4 /g of dried soil within 20 min incubation at 37 °C. The mean annual activity of each of these enzymes was calculated.

Measurement of lycorine content

Conditions used in assays with high-performance liquid chromatography (hplc).

HPLC was used to measure of lycorine content. The chromatographic conditions used were set as following: 20 μL of samples or standards were injected into the Agilent Eclipse XDB-C18 column at 25 °C and eluted with mobile phase of 0.1% phosphoric acid:methanol of 65:35 at flow rate of 1.0 mL/min. The detection wavelength was at 288 nm 24 .

Linear regression

Lycorine content was measured with a LC-20AT HPLC (Shimadzu, Japan). 20 μL of lycorine standard (HPLC ≥ 98%, National Institutes for Food and Drug Control) solutions at concentrations of 20.0, 40.0, 60.0, 80.0 and 100.0 μg·mL −1 were injected into the column and separated under the above conditions. The equation of linear regression was as follows: y  = 20648x + 11934, R 2  = 0.9996. The chromatogram of the lycorine reference substance was shown in Fig. 1a . Its retention time of the objective peak was 5.833 min.

Sample preparation and measurement of lycorine content

The sieved samples of the bulbs were dried at 65 °C to constant weight. The sample was extracted with Soxhlet method 24 . The sample solution was separated as described above and lycorine content was calculated using the peak area according to the linear regression equation.

Data analysis

Data analysis was performed with Statistical Product and Service Solutions(SPSS). The correlation analysis was conducted with Pearson correlation coefficient method. The key soil factors influencing P n , biomass and lycorine content of L. aurea were determined with multiple regression analysis 42 and path analysis 43 , 44 . The multiple regression analysis was performed with a stepwide method to sequentially include variables in the model, using the following pre-established criteria: inclusion of a variable when its level of significance was <0.05 (p in <0.05), exclusion of a variable when its level of significance was >0.10. This method selects significant variables one by one, and every time a new variable is included, the rest of those previously selected are examined to check if any of them may be removed from the model. The significance of coefficients was evaluated by a t-test. A p-value < 0.05 was considered significant.

Additional Information

How to cite this article : Quan, M.H. and Liang, J. The influences of four types of soil on the growth, physiological and biochemical characteristics of Lycoris aurea (L’ Her.) Herb. Sci. Rep. 7 , 43284; doi: 10.1038/srep43284 (2017).

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Material


This work was supported by National Natural Science Foundation of China (No. 31470403), Innovation Platform Open Fund in Higher Education Institutions of Hunan Province (No. 11K051) and the Foundation of Hunan Key Discipline Construction Projects. We sincerely thank Dr. L.J. Ou, A.P.A.N. He and A.P.S.H. Li for their helps in the experiments, Prof. X.J. Wu and Prof. C.W. She for the helpful discussions and constructive suggestions.

The authors declare no competing financial interests.

Author Contributions M.H.Q. designed the study, analyzed data and wrote the paper; J.L. performed experiments and analyzed the data. All the authors reviewed and approved the manuscript.

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  21. Plants distinguish different photoperiods to independently control

    Arabidopsis thaliana grows faster in long days, so we mined transcriptomic data for genes that are induced in long days and required for proper vegetative growth. We identified MYO-INOSITOL-1-PHOSPHATE SYNTHASE 1 (MIPS1), which encodes a gene necessary for plants to produce myo-inositol, a sugar required for a variety of important cellular processes that control growth.

  22. Plant size‐dependent influence of foliar fungal pathogens promotes

    New Phytologist is an international phytology journal owned by the New Phytologist Foundation publishing original research in plant science and its applications. Summary The effect of pathogens on host diversity has attracted much attention in recent years, yet how the influence of pathogens on individual plants scales up to affect community ...

  23. Application of ethanol alleviates heat damage to leaf growth and yield

    1 Plant Genomic Network Research Team, RIKEN Center for Sustainable Resource Science, Yokohama, Kanagawa, Japan; ... Heat stress damages plant growth and yield (Hoshikawa et al., 2021; Ahmad et al., 2022). ... In this paper, we investigated whether ethanol application enhances heat stress tolerance in tomato 'Micro-Tom'. ...

  24. The Effects of Magnetic Fields on Plants Growth: A ...

    Plant Growth The Effects of Magnetic Fields on Plants Growth: A Comprehensive Review International Journal of Food Engineering 5 (1):79-87 Authors: Neo E Nyakane Central University of...

  25. 3D Printed Materials Characterization for Rapid Prototyping and Plant

    Space Biology experimentation but their effects during plant growth and sanitation have not been documented. With further testing we can determine how certain 3D printed materials affect our plants. The way we tested germination included laying two pieces of germination paper down with the printed petri dish insert of the various material and 14 seeds of Outrageous lettuce to fit in the holes ...

  26. Effects of different fertilization rates on growth, yield, quality and

    Abstract To select the optimum fertilizer application under specific irrigation levels and to provide a reliable fertigation system for tomato plants, an experiment was conducted by using a microporous membrane for water-fertilizer integration under non-pressure gravity.

  27. In Memoriam: Graeme Berlyn, E. H. Harriman Professor of Forest

    Graeme P. Berlyn, a world-renowned expert on the anatomy and physiology of plants and trees, died Feb. 16 in Hamden at the age of 90. Berlyn, whose breadth of research included wood anatomy, plant embryology, tissue culture, biotechnology, and the morphology and physiology of trees and forests in relation to environmental stress, taught at YSE for more than 60 years.

  28. Climate Change, Population Growth, and Population Pressure

    We find that standard population growth projections imply larger reductions in income than even the most extreme widely-adopted climate change scenario (RCP8.5). Climate and population impacts are correlated across countries: climate change and population growth will have their most damaging effects in similar places.

  29. The influences of four types of soil on the growth, physiological and

    Lycoris aurea (L' Her.) Herb (L. aurea), also known as Golen Magic Lily, is a perennial herbaceous plant belonging to the genus Lycoris.It is a traditional Chinese medicinal herb plant 1.Its bulb is rich in more than 10 types of alkaloids, including lycorine, galanthamine and lycoramine etc. and can be used to treat several important diseases such as poliomyelitis sequel, Alzheimer's ...