JXB Advance Access originally published online on October 3, 2005
Journal of Experimental Botany 2005 56(421):2777-2782; doi:10.1093/jxb/eri297
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OPINION PAPER |
Is a physiological perspective relevant in a ‘genocentric’ age?*
1Agronomy Physiology Laboratory, PO Box 110965, University of Florida, Gainesville, FL, 32611-0965, USA
2Department of Crop, Soil and Environmental Sciences, University of Arkansas, 1366 W. Altheimer Drive, Fayetteville, AR 72704, USA
To whom correspondence should be addressed. Fax: +1 352 392 6139. E-mail: trsincl{at}ifas.ufl.edu
Received 21 June 2005; Accepted 22 August 2005
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Abstract |
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 Top Abstract IntroductionPlant physiology and the...Genocentric disconnect with...Genocentric disconnect with...A return to Shull's...References |
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Currently, the major thrust of plant physiology research is to identify and understand the regulation of genes that might be relevant in plant development and growth. The dominance of a genocentric view of plant behaviour has, unfortunately, resulted in the development of major disconnects in the classical view of plant physiology as a partnership between fundamental and practical research contributing to improved plant production. One disconnect is that much of the genocentric research appears to be organized and executed without regard to the practical needs of enhancing plant performance under applied conditions. Although practical benefits from genocentric research are often claimed, basic assumptions guiding much research and the experimental protocols used are commonly not relevant for real-world plant production. A second disconnect is a failure fully to appreciate the lessons learned in 40 years of classical plant physiology research concerning the role of physiological processes in altering whole plant performance. Regulation of plant systems has proved to be complex and redundant. Alteration of a single physiological process is compensated or dampened so that commonly very little change in plant growth and yield results from modification of a single physiological process. Based on a few successful projects employing classical plant physiology to achieve crop yield increase, key characteristics for research projects that truly seek to increase plant performance in production systems are identified. Basically, the partnership between the fundamental and practical research long espoused for plant physiology needs to be re-established in an intimate and meaningful way.
Key words: Classical plant physiology, genocentric research, plant development, plant growth
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Introduction |
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TopAbstractIntroductionPlant physiology and the...Genocentric disconnect with...Genocentric disconnect with...A return to Shull's...References |
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A key mission of science is to examine the disorderly, even chaotic appearance of nature, and develop overarching descriptions for defined segments of that nature. Out of necessity many of the concepts will be abstract simplifications of reality, but if they describe a substantial part of that reality then concepts are often retained as useful working hypotheses. Sometimes a concept is so compelling and complete in its ability both to describe and predict unforeseen aspects of nature that it is elevated to the level of a theory. (In spite of the claim of creationists in arguing against evolution as only a theory, a scientific theory connotes an extremely high degree of consistency with observations and experimental results.) Hypotheses and theories provide the framework for investigations leading to the next stage of scientific interpolation and extrapolation.
Consequently, current concepts of science have a large impact on the perception of nature. While reality remains reality, the consequences of the concepts used to describe nature can have a large impact on the direction of human understanding. An illustration of this situation is the geocentric view of our solar system that was accepted for centuries by the world's leading thinkers. Geocentric models involving elaborate families of circular orbits worked quite well for the people of that time in describing the movement of the planets in the sky. Only when Copernicus, Kepler, and Galileo obtained more precise observations and opened the discussion on planetary movement were the limitations of the geocentric model exposed. The heliocentric theory eventually replaced the geocentric view as the improved description of the solar system.
A worry for those of us involved in plant physiology is to consider that we may have moved to something like a geocentric stage in examining the workings of higher plants. In our case, we are now dominated by a ‘genocentric’ view of evaluating plant growth, development, and responses to the environment. Our journals are filled with attempts to identify genes that might explain physiological responses within the ‘orbits’ of the genocentric perspective. This view is fostered by the description often used by the popular press that DNA and genes are the ‘blueprint’ of life. The blueprint analogy of the genocentric perspective implies that organism development, like the construction of a building, proceeds according to the rigid specifications laid down in the DNA. If a plant's DNA calls for a plant to grow long roots, then the plant grows long roots.
In reality, the analogy of the genetic code as a blueprint to describe plant development and growth is misleading. A better analogy may be that DNA and genes are more like the prompt-script given to comics at an improvisational club. The prompt-script can be accurately reproduced in a photocopy machine and the same prompts can be given to the performers every night. However, the performance unfolds on any given night according to the imagination and wit of the comics together with the reaction of the audience. That is, the prompts give a general direction and perhaps indicate boundaries but the unfolding of an individual performance depends on both the immediate and general ‘circumstances’ that exist at the time of the performance. So too with plants, the development and growth of plants is to a large extent an emergent product within the boundaries of the gene code and the contingencies in the code. The ultimate expression of the code is dependent on the specific biotic and abiotic environment in which cells and organs find themselves as they develop and grow.
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Plant physiology and the genocentric perspective |
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TopAbstractIntroductionPlant physiology and the...Genocentric disconnect with...Genocentric disconnect with...A return to Shull's...References |
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Are there serious implications for those of us working on the physiology of plants whether we view our world from the genocentric perspective or from the view that DNA is the prompt-script impacted by a whole range of environmental factors resulting in emergent properties of the whole plant? The answer is clearly ‘yes’ because the research undertaken and the experiments selected are directly dependent on the investigator's view of reality. The genocentric view has caused a preponderance of plant physiological research to focus on genes and DNA as the ultimate description of plant life. However, this view is rather new and eclipses the perspective during the first half-century of research in plant physiology. The classical view of plant physiology research was clearly outlined by Charles A Shull in the Forward of Vol. 1 of Plant Physiology (1926),
‘Research in plant physiology must proceed in two general directions. It must continue to spread out into the practical fields of human service, such as agriculture, horticulture, agronomy, ecology, pathology, forestry, climatology, and medicine. At the same time it must constantly delve more deeply into the problems of developmental metabolism under the leadership of physiologists well trained in the methods of biophysics and biochemistry. ... These two lines of investigation, practical and fundamental, must always go hand in hand. There can never be a logical separation of these two aspects of our science.’
The fundamental side of Shull's partnership has been well-served in the past by reductionist research in plant physiology and certainly continues as a dominating force. The problem is that there seems to be very little of the ‘hand in hand’ partnership between the fundamental and practical envisioned by Shull. Over the past 40 years the research of plant physiologists has shifted to probing deeply into the genetic code for an understanding of biochemical traits that might be altered to increase plant production.
Although empirical plant breeding coupled with improved plant husbandry has resulted in greatly increased crop yields, there has been little success in increasing potential crop yield that can be directly attributable to either classical plant physiology or genocentric research. Only a few rare cases exist in which plant physiological investigations encompassed a description of a problem, identification of superior genetic resources, and development of commercial germplasm (Sinclair et al., 2004
; Campos et al., 2004). No doubt there have been spectacular advances in knowledge of how plants function, but one of the lessons from this research is that plants have substantial redundancy in regulation and tend to be homeostatic (Edmeades et al., 2004). However, it has not been easy to ‘convince’ plants in targeted physiological studies to set aside the successes of evolution and function in the manner desired in agriculture. The few successes originating from classical plant physiology offer important lessons about the characteristics of the research effort that are required to apply ‘fundamental’ information to ‘practical’ problems. Unfortunately, these lessons point to widening disconnects between the reality of plant performance in the cropping environment and genocentric research.
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Genocentric disconnect with practical reality |
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TopAbstractIntroductionPlant physiology and the...Genocentric disconnect with...Genocentric disconnect with...A return to Shull's...References |
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Preambles of many grant proposals and papers, and certainly the continuing theme of the popular press, focus on molecular genetics as the basis for expecting remarkable progress in increasing crop yields. Nevertheless, at several levels there often seem to be major disconnects between genocentric research and what is required to achieve improved plant performance at the practical level. To illustrate this disconnect, the specific topic of improving plant performance under water-deficit conditions is examined. This is an area of our personal research interest and drought tolerance is almost invariably listed in the litany of anticipated benefits of genocentric research.
While improved plant performance under water-limited conditions would be a huge contribution, much of the actual research reflects serious misunderstandings about the fundamental limitations of water in the agricultural environment and what is needed to increase crop yields. Below, four questions are addressed that help to illuminate disconnects between the genocentric view of water-deficit research and the requirements for practical benefit.
Is drought survival a concern for most agricultural species?
Commonly, the key experimental test/screen for drought tolerance among transformed lines is an ability to survive severe stress. In fact, plant traits required for drought survival are rather unique and tend to be expressed so that whole-plant water status is altered (Sinclair, 2000). Most importantly, screens for drought survival are essentially irrelevant in agriculture. High cash-value crops such as vegetables and fruits are almost universally grown under conditions where water is reliably available so water-deficits of any type are not common for many of these crops. Drought survival for tomato, for instance, is not an agricultural issue.
On the other hand, water-limited conditions are very common in annual grain crops and water deficits are often the major source of yield loss. However, significant yield loses are very rarely a direct result of a failure to survive drought. Drought-survival traits are not important because if water deficits are sufficiently severe and prolonged to threaten crop survival, yields will necessarily be extremely low and economically devastating to the grower. Survival of a crop is virtually irrelevant in annual grain crops. Instead, agriculture will be benefited by improved exploitation of the available water before crops are subjected to severe drought. Consequently, it is expected that genocentric research based on tests/screens for drought tolerance as plant survival will have little to offer agriculture.
Does osmotic adjustment offer benefits for crop improvement
It seems intuitive that a viable plant that continues growth under water-deficit conditions as a consequence of osmotic adjustments in the plant cells is a desirable phenotype. In fact, this is not the case because, as soil water supply is getting low, plants need to protect themselves from further, rapid use of water. Stomata closure and a stoppage of plant growth are desirable to minimize further water loss and an even worsening of the water-deficit situation. Consequently, osmotic adjustment, which is often offered as a solution to drought stress, is anticipated to benefit crops only rarely. Indeed, there is a long history of study on osmotic adjustment in crops and virtually all studies have shown osmotic adjustment to be a neutral or negative trait for increasing crop performance (Serraj and Sinclair, 2002). Out of the large number of studies on osmotic adjustment, two cases (Santamaria et al., 1990; Morgan, 1995) are often cited as the key evidence for yield benefit from osmotic adjustment, but both of these cases are sufficiently unique that they offer virtually no support for general application.
It is possible that osmotic adjustment in root tips could be an advantage if the adjustment allows root growth into wet soil that is currently not being exploited. Even this solution has its limitations because rooting depth may be limited by soil properties and the deep soil layers to which the roots might grow must be recharged with water between cropping seasons. A one-time extraction of deep soil water that is rarely recharged offers no long-term solution to drought stress. Therefore, a careful analysis of specific environments is required to determine if even osmotic-induced root growth would bring sustained benefit.
Are there universal genetic traits to increase yields under water-deficit conditions?
Plant response to water-deficit conditions actually depends both on the interaction among a very large number of plant traits at all levels of organization from the molecular level through to the whole plant, and on a number of factors in the physical environment. The dynamic interaction of plant and environment variables makes the rate of water use an emergent property of those particular circumstances. The rate of water use to a large extent defines the nature of the water deficit and the response of plants to the stress. Consequently, there is usually not a single factor that controls crop response to developing drought but rather, a number of variables are collectively involved in influencing the ultimate impact of water deficit on crop performance. The consequences of various plant traits and environmental conditions have to be evaluated in the specific environments in which the crop is to be grown, that is field evaluations (Condon et al., 2004).
Sinclair and Muchow (2001) reported a simulation analysis of the impact of yield over a 20-year period in a single location in response to altering a number of plant traits that have putative benefit for water-limited environments. Except for increased rooting depth, the yield response to all traits was quite variable, with yields being increased or decreased in any given year depending on the weather scenario. A trait that offers a mean increase in yield over a number of years but suffers yield loss in a few years will not be of use for growers. Similarly, a trait resulting in increased yield for locations in a field that sometimes suffer drought is unacceptable if the trait also causes lowered yields in the better locations in the field (Campos et al., 2004).
What laboratory tests are required to mimic water deficits suffered by field crops?
The genocentric perspective has resulted in experimental methodologies that are disconnected from real-world issues. It has already been mentioned that tests/screens for genes that confer drought survival are essentially irrelevant to agriculture. More complex alternative screens that have been used in genocentric research turn out, in many cases, to be selections for traits associated with water conservation. Selected plants that use water more slowly will retain more water in the soil after a fixed amount of time and, therefore, the plants will appear more ‘attractive’. Decreased transpiration rates due to decreased stomata conductance or smaller plant leaf area, for example, allow plants to appear more attractive in a water-deficit screen, but the advantage comes as a result of slower growth rate. As discussed above, drought ‘tolerance’ achieved at the expense of growth rate, and consequently lower yields when water is more plentiful, is not acceptable to growers.
Another factor often overlooked in genocentric experiments is that the method of imposing water deficit has a large influence on plant response. For example, plants are often grown on artificial media that include peat moss and/or vermiculite. These materials have hydraulic conductance that substantially differs from mineral soils. Wahbi and Sinclair (2005) found that the pattern of water-deficit stress imposed on plants grown on artificial soil is very different from water-deficit stress resulting from drying of mineral soil. Further, dehydration techniques such as rapid drying of the soil within a few days, or even complete removal of plants or leaves from water sources, are not relevant to real-world scenarios where deficits develop over a three- to four-week period, which allows time for acclimation at both the organ and gene level (Campos et al., 2004). Gene activity as a consequence of drying over a few hours or even a few days may well be quite different from that expressed by plants in a cropping environment.
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Genocentric disconnect with history |
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TopAbstractIntroductionPlant physiology and the...Genocentric disconnect with...Genocentric disconnect with...A return to Shull's...References |
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Plant physiologists over the past 40 years have made remarkable advances in understanding individual physiological traits. Indeed, this research has contributed greatly to the ability to explore genes and their behaviour. In addition, exploration of the physiological traits in modern, high-yielding lines derived from empirical crop breeding has given great insight about the factors that have contributed to yield increase. Many elegant genocentric studies are underway to investigate enhancing those traits that have been investigated in the past: drought-stress tolerance, increased photosynthesis rates, improved nitrogen efficiencies, and altered seed growth characteristics. Unfortunately, in many cases the full scope and implications of results obtained from classical plant physiological investigations are seemingly being overlooked.
For example, photosynthesis was extensively studied as a trait that might be enhanced to increase crop yield. Genetic variability in leaf photosynthetic activity was identified and found to be heritable, but no yield benefits were found. One lesson from that research was that superior physiological performance of a trait at a lower level diminished at each higher level of complexity leading to crop yield. That is, yield is an emergent trait responding to a number of genes and confounding factors in the plant and surrounding environment. This can be illustrated by examining the consequence of increasing photosynthetic capacity at the molecular level and tracking the impact through hierarchical levels up to crop yield (Fig. 1). Sinclair et al. (2004) presented such a calculation starting with a fictitious promoter that resulted in a 50% increase in RNA synthesis for each subunit of Rubisco. The consequence of such a hypothetical molecular change was calculated through the hierarchal chain, leading to soybean yield based on experimental evidence obtained at each step, progressing from the assumed promotion of RNA synthesis in leaves, stimulation of Rubisco content, change in leaf photosynthetic rate, improved photosynthetic rate of isolated plants, and finally increased mass accumulation by a crop. Through this chain the assumed 50% promotion of RNA synthesis is diminished to only an 18% increase in crop mass.
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The key final step is to estimate the impact of altered mass accumulation on seed yield. This calculation illustrates that there is more than one stream of inputs that influence crop yield. Soybean seeds are high in protein content so nitrogen for increased seed growth must also be accumulated and stored in the plant for eventual use in generating seed yield. Depending on assumptions about the physiological impact on plant nitrogen accumulation associated with the increase in photosynthetic activity, grain yield was calculated either to increase by 6% or decrease by 6%. It is not surprising that many years of intensive investigation of increasing photosynthetic capacity have not resulted in increased crop yields.
The complexity of emergent properties influencing crop yield make the linkage between gene modifications and yield a very tenuous one. Research over the past 40 years has shown the difficulty in increasing crop yield by simple selection and breeding for only a specific, target trait. The genocentric perspective does not break this reality and, in fact, tends to move further away from the emergent properties of crops by penetrating further into molecular activity. The challenges of the past remain, and may even be amplified by the ability to expand our understanding into even greater complexity.
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A return to Shull's model of plant physiological research |
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TopAbstractIntroductionPlant physiology and the...Genocentric disconnect with...Genocentric disconnect with...A return to Shull's...References |
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One critical outcome of classical plant physiology studies is that there have been very few successes in transferring physiological knowledge to improved crop performance. Failure to contribute more to practical solutions is traced to the need for sustained physiological research effort through all the steps leading to commercial success starting with studies of basic physiological processes, then developing and executing successful searches for genotypes with improved physiological performance, and finally tracking of traits in breeding lines.
Fortunately, there are a few rare cases where crop improvement has resulted from fundamental physiological research contributing basic information about physiological activity, participating in selection of superior germplasm, and supporting the breeding for superior performance (Sinclair et al., 2004). These few cases of success did not hinge particularly on brilliant physiological insights but rather followed a path closely aligned with CA Shull's charge that plant physiological research must advance ‘hand in hand’ with a balance between the fundamental and practical. Consistent with Shull's views, we (Sinclair et al., 2004) identified four critical characteristics common to those physiological programmes that ultimately generated commercially useful germplasm.
- (i) An early step, even the initial step, of the research was to investigate, under field conditions, whether an alteration in a trait would truly be of benefit to a crop (see also Edmeades et al., 2004; Campos et al., 2004).
- (ii) Techniques for phenotyping traits were developed because it is necessary to assess the performance of a specific trait, i.e. a genotype, under a range of environmental conditions (see also Ishitani et al., 2004
). As pointed out by Edmeades et al. (2004), many differences at the gene sequence level result in only subtle phenotypic effects.
- (iii) Multidisciplinary teams were formed that included expertise in physiology, genetics and breeding, and agronomic management.
- (iv) Long-term commitment to achieving yield increase was made by members of the research team and by funding entities. The successful projects each required 12–15 years of effort. Integrating a team of scientists and providing sustained funding is likely to be the most challenging aspect in today's research environment.
- (ii) Techniques for phenotyping traits were developed because it is necessary to assess the performance of a specific trait, i.e. a genotype, under a range of environmental conditions (see also Ishitani et al., 2004
). None of the characteristics summarized above for physiological efforts to improve crop plants can be ignored as a result of advances in molecular genetics. In fact, the need for each of the above characteristics is likely to be even more demanding because molecular investigations add another layer of complexity and understanding of how plants work.
To answer the question posed in the title of this paper: 'Is a physiological perspective relevant in a genocentric age?, our conclusion is a resounding yes. Indeed, those with expertise in classical plant physiology may have the pivotal role in achieving the agricultural benefits envisioned by CA Shull. The genocentric approach offers new germplasm and understanding, but the emergent nature of yield from physiological processes demands that all components contributing to yield be considered. It is those scientists that have the understanding of interactions within plants and between plants and dynamic environments that can provide the key link between gene activity and crop yield.
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Footnotes |
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* This paper was presented by invitation at the 2005 Kriton Hatzios Symposium of the Southern Section of the American Society of Plant Biologists. Florida Agricultural Experimental, Journal Series No. R-10954.
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References |
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TopAbstractIntroductionPlant physiology and the...Genocentric disconnect with...Genocentric disconnect with...A return to Shull's...References |
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Campos H, Cooper M, Habben JE, Edmeades GO, Schusser JR. 2004. Improving drought tolerance in maize: a view from industry. Field Crops Research 90, 19–34.
Condon AG, Richards RA, Rebetzke GJ, Farquhar GD. 2004. Breeding for high water-use efficiency. Journal of Experimental Botany 55, 2447–2460.
Edmeades GO, McMaster GS, White JW, Campos H. 2004. Genomics and the physiologist: bridging the gap between genes and crop response. Field Crops Research 90, 5–18.[CrossRef]
Hammer GL, Sinclair TR, Chapman SC, van Oosterom E. 2004. On systems thinking, systems biology, and the in silico plant. Plant Physiology 134, 909–911.
Ishitani M, Rao I, Wenzl P, Beebe S, Tohme J. 2004. Integration of genomics approach with traditional breeding towards improving abiotic stress adaptation: drought and aluminum toxicity as case studies. Field Crops Research 90, 35–45.[CrossRef]
Morgan JM. 1995. Growth and yield of wheat lines with differing osmoregulative capacity at high soil water deficit in seasons of varying evaporative demand. Field Crops Research 40, 143–152.
Santamaria JM, Ludlow MM, Fukai S. 1990. Contributions of osmotic adjustment to grain yield in Sorghum bicolor (L.) Moench under water-limited conditions. I. Water stress before anthesis. Australian Journal of Agricultural Research 41, 51–65.
Serraj R, Sinclair TR. 2002. Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant, Cell and Environment 25, 333–341.[CrossRef][Medline]
Sinclair TR. 2000. Model analysis of plant traits leading to prolonged crop survival during severe drought. Field Crops Research 68, 211–217.
Sinclair TR, Muchow RC. 2001. System analysis of plant traits to increase grain yield on limited water supplies. Agronomy Journal 92, 263–270.
Sinclair TR, Purcell LC, Sneller CH. 2004. Crop transformation and the challenge to increase yield potential. Trends in Plant Science 9, 70–75.[CrossRef][Web of Science][Medline]
Wahbi A, Sinclair TR. 2005. Differing transpiration response to drying of artificial and mineral soils. Environmental and Experimental Botany (in press).
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