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a Agronomy Dep., Univ. of Florida, Gainesville, FL 32611-0500
b Univ. of Florida, Agronomy Physiology and Genetics Laboratory, Gainesville, FL 32611-0965
* Corresponding author (kjb{at}ifas.ufl.edu)
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 TOP ABSTRACT INTRODUCTIONTHE FULL CIRCLE OF...SIGNIFICANT DISCOVERIES OF CROP...Improved Understanding of Crop...THE PRESENT AND THE...REFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONTHE FULL CIRCLE OF...SIGNIFICANT DISCOVERIES OF CROP...Improved Understanding of Crop...THE PRESENT AND THE...REFERENCES |
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A concern in meeting the anticipated needs for future whole-plant studies is that the recognition of the critical role of the crop physiological perspective may come after the current momentum in the higher level, whole-plant perspective has been lost. We believe there has been a decline in C-2 membership, especially the whole-plant specialists, concurrent with the initiation and rise in membership in the C-7 (Genomics, Molecular Genetics, and Biotechnology) division. There is no doubt of the benefit of molecular genetics to help tease out specific functions and processes. Nevertheless, this approach has danger as well because translation of these research results into an appreciation of the whole-plant function under field environmental stress conditions is extremely difficult, as evidenced by the historical, long cycle of physiological perspective.
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THE FULL CIRCLE OF CROP PHYSIOLOGY RESEARCH |
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TOPABSTRACTINTRODUCTIONTHE FULL CIRCLE OF...SIGNIFICANT DISCOVERIES OF CROP...Improved Understanding of Crop...THE PRESENT AND THE...REFERENCES |
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1969–1970: Landmark Years and an Optimistic Start
The crop physiology meeting in Lincoln, NE, in 1969 which led to the book Physiological Aspects of Crop Yield, was a time of particular excitement. The Nebraska meeting and book marked the beginning of putting individual physiological processes together into a holistic view of the crop. The emphasis was at the physical level, where the physics of gas exchange and light interception in crop stands and the potential impact on yield was described at that meeting by a brilliant group of converted physicists and physiologists: Edgar Lemon, Cornell University; John Monteith, University of Nottingham; Bob Loomis and William A. Williams, University of California–Davis (Lemon, 1969; Loomis and Williams, 1969; Montieth, 1969).
There were also discussions of genetic variation for key physiological traits, even though none were yet being applied directly in breeding programs. Those subject areas included the full discovery and resolution of the C-4 photosynthesis pathway, the explanation for photorespiration in C-3 plants, water relations, translocation and phloem loading, as well as assimilate transfer processes in seeds and sinks, N metabolism and fixation, global climate change effects (CO2 and temperature), and physiological basis for genetic yield potential. Robert Chandler (International Rice Research Institute) discussed morphology, stand geometry, and N relations of old vs. new dwarf rice cultivars and gave an explanation of the impact of the Green Revolution (Chandler, 1969).
Less than a year after the Nebraska meeting, Norman Borlaug won the Nobel Peace Prize in 1970. This award was exhilarating for all crop scientists and gave us all certification that what we were doing was important and that tremendous progress had been made in meeting the need to feed a hungry world.
Physiological Basis of Genetic Yield Potential
From the mid-1960s through the 1990s, crop physiologists contributed significantly to the understanding of yield physiology from the viewpoint of whole-plant physiology. This era of increased whole-plant understanding of crop physiology is illustrated by papers presented at the First International Crop Science Congress held in July 1992 at Ames, IA, and the Symposium on Physiology and Determination of Crop Yield held in June 1991 at Gainesville, FL. The First International Crop Science Congress was an important outlet for presentations on whole-plant physiology, although commercial cultivars resulting from physiology research were not reported. Lloyd Evans presented a plenary paper that developed an optimistic case for continuing increases in crop yields based on improvements in physiological characteristics (Evans, 1993). On the other hand, Sinclair (1993), in his response slot after the Evans talk, discussed limitations on yield potential increase, as illustrated by the well-known Jack in the Bean Stalk story (Sinclair, 1993). Sinclair's viewpoint was that yield could not be increased by using "magic beans" (e.g., molecular genetics) that grew overnight without light, fertilizer, water, or time resources. His message was that there were real limits in resources that constrain genetic improvement of yield.
The book Physiology and Determination of Crop Yield represented the state of the art for cellular, leaf-level, and whole-plant physiology, before the advent of the major shift to molecular genetics research. Authors of chapters in this book demonstrated a good understanding of whole-plant physiology. Other authors thoroughly summarized the literature describing how plant growth processes were affected by stresses of water deficit, cold stress, heat stress, air pollutants, and ultraviolet irradiance. Another group of authors, led by Evans (1994), Boote and Tollenaar (1994), Austin (1994), and Sinclair (1994), described the physiology of yield potential relative to genetic traits and resource limitations.
This book probably represented the zenith of the era of understanding and integrative synthesis of whole-plant physiology, before the beginning of the molecular genetics era of fragmented targeting of individual elements of physiology associated with either inserted transgenes or markers for genes. We are still in this new era, with just a glimmering of understanding of the need to again concern ourselves with the whole-plant integration of physiological processes. A new breed of researchers is working on functional genomics, but the work is being done on isolated plant processes with an agronomically unimportant weed, which may have few features at the whole-plant level that correspond to high crop productivity.
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SIGNIFICANT DISCOVERIES OF CROP PHYSIOLOGISTS OVER 50 YEARS |
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TOPABSTRACTINTRODUCTIONTHE FULL CIRCLE OF...SIGNIFICANT DISCOVERIES OF CROP...Improved Understanding of Crop...THE PRESENT AND THE...REFERENCES |
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Resolution of the nature of photorespiration of crop plants was another important advance for physiological studies. George Bowes, now at the University of Florida, and Bill Ogren, at the University of Illinois, discovered that the ribulose bisphosphate carboxylase enzyme (Rubisco) was also an oxygenase enzyme (Ogren and Bowes, 1971). This discovery came about from practical questions addressed toward increasing yields of soybean (Ogren and Bowes, 1971; Laing et al., 1974, described in Ogren, 1984).
Integration of Leaf to Canopy Assimilation to Production
The role of single-leaf photosynthesis integrated to canopy assimilation was highlighted by a group of physiologists and modelers to the present (deWit, 1965; Duncan et al., 1967; Norman and Arkebauer, 1991; Boote and Loomis, 1991; Boote and Pickering, 1994; DePury and Farquhar, 1997; Lizaso et al., 2005). This placed the perspective away from strictly leaf photosynthesis per se, back to the whole picture of leaf area index, light interception, diffuse and direct beam irradiance, leaf N status, leaf angle, and solar angle. Good understanding of the separate roles of respiration for growth and maintenance respiration purposes was made by Penning deVries and McCree (McCree, 1974; McCree and Silsbury, 1978; Penning deVries, 1975; Penning deVries et al., 1974), and again the emphasis was placed back on the whole crop function, rather than the oversimplified view that respiration was merely a wasteful process.
The integration from leaf to canopy assimilation, and to season-long growth and yield, has taken the bloom off the more publicized concept of increasing leaf photosynthesis. Why do we say this? First, increases in single leaf light-saturated rate of 10%, for example, translate into much less at canopy level (5% or less) under high-light conditions, which is the best possible if there are no negative linkages such as increased leaf rate being linked to decreased specific leaf area which reduces the benefit to 2–3% (Boote and Tollenaar, 1994). Finally, when such leaf traits are simulated in the leaf-to-canopy scaling inside crop growth models, we begin to see that many other traits have more important effects that integrate C gain into growth and yield. Other yield-influencing traits include specific leaf area and the leaf area index, which influence light interception, duration of vegetative growth, duration of reproductive growth, partitioning intensity, and so forth (Boote and Tollenaar, 1994).
Water Relations and Growth Physiology
The 1970s and 1980s spanned an era of discovery and documentation of the mechanistic basis of crop–water relations (Boyer, 1969, 1976; Hsaio, 1973). A number of crop physiologists, including Krieg, Sullivan, Bennett, and Sinclair, contributed to this effort. During this time, understanding of plant water potential and its components were well developed and tested, but new findings peaked by the late 1980s. Then, by the early 1990s, a group of crop physiologists, led by Davies et al. (1990), Zhang and Davies (1990), Davies and Zhang (1991), and Tardieu et al. (1992) discovered the strange phenomena of roots in drying or high impedance soils sending growth regulator signals (abscisic acid) to shoots that limited stomatal conductance, photosynthesis, and expansive processes, irrespective of the hydraulic status of shoot tissue. Thus, there is more to crop–water relations than simple hydraulics and plant–water potential, as these signals are redundant to water-relations hydraulics and co-regulate plant water status. Processes of leaf and shoot expansion and their sensitivity to water relations, light, cellular processes, and root-to-shoot signals were reviewed by Van Volkenburgh (1994).
Others studied the elongation phenomenon at the growing meristem of roots (Sharp, 1994; Sharp et al., 1990) or leaves (Schnyder and Nelson, 1988), and investigated the role of phloem unloading to create micro-osmoregulation at the meristematic region relative to the tissue expanding zone. Concurrently, Cosgrove (1986, 1999) discovered the role that expansin enzyme proteins in that elongation zone play to promote or limit cell wall elongation, again dependent only partly on cellular water relations (turgor).
Nitrogen Metabolism and Symbiotic N2–Fixation
Beginning in the 1960s and for the next 25 yr, Hageman's group at the Univ. of Illinois studied the role of nitrate reductase in N metabolism and yield (Hageman and Flesher, 1960; Hageman, 1979; Hageman and Lambert, 1988). Despite the obvious importance of N to yield potential, these detailed studies and attempts for genetic selection of superior performance for nitrate reductase failed to lead to significant yield improvement (Hageman and Lambert, 1988). Also, the focus on a single enzyme failed to result in developing a holistic overview of N metabolism (Harper, 1994). The lack of impact on crop productivity from this research focused on the performance of a single enzyme seems to carry an important lesson for the current molecular perspective for increasing yields.
The pathways and mechanisms of N2–fixation, as well as environmental and assimilate requirements for it, have been well elucidated during the past 30 yr (see Layzell and Moloney, 1994). We now know much more about the environmental and the plant internal mechanisms that regulate N2–fixation; nevertheless, we have not been able to substantially improve on the N2–fixation mechanism in the important legumes such as soybean. The process is apparently under exquisite control, fixing more N2 if mineral N is not taken up, but the plant does not fix more than the current N demand. In the mid-1980s, there was some thought that hydrogenase-uptake-positive (hup) bradyrhizobium (Eisbrenner and Evans, 1983) might give a yield boost, but this could not be shown in field tests.
On the other hand, progress has been made in overcoming the important limitation of only modest soil drying on the N2–fixation rates of soybean (Serraj et al., 1999). Now, genotypes have been identified that have N2 fixation that is tolerant of soil drying (Sall and Sinclair, 1991; Sinclair et al., 2000). Some of these genotypes have been used in a breeding program and cultivars have been identified that outyield commercial checks under rainfed conditions (Chen et al., personal communication, 2005).
Phloem Loading, Phloem Unloading, and Determinants of Seed Growth and Sink Strength
Translocation, for example, was thoroughly investigated by Geiger and his students and they confirmed the hypothesized activated-mass-flow hypothesis in source tissues (Geiger and Giaquinta, 1982; Giaquinta, 1983). These researchers also showed that the translocation pathway itself was not really the most important regulating feature, but rather that the direction of transport (and thus partitioning) was regulated by activity of sinks and sources. The mechanisms of unloading, transfer, and subsequent storage of assimilate in sink tissues of seed or tuber or stalk or tap root, all of the "push–pull" variation according to Geiger, was well-studied and nicely summarized in the review by Thorne (1985). Other researchers discovered the unloading and loading mechanisms into mature vegetative sink cells of sugarbeet (Beta vulgaris subsp. vulgaris) taproots (Wyse, 1979) and sugarcane (Saccharum officinarum L.) internode cells (Lingle, 1989). Volenec et al. (1996) have continued to study assimilate transfer of C and N reserves into storage cells of alfalfa taproots. The unloading process into vegetative meristems, according to Geiger, is of the "push–no pull" type of symplastic transfer, and has not been as widely studied, although expansive growth of vegetative organs was studied by Jerry Nelson and students (Schnyder and Nelson, 1988).
The principles of genetic, nutritional, and environmental determinants of seed growth rate and duration were systematically researched and published by Egli (1998), who published a book on the topic entitled Seed Biology and the Yield of Grain Crops. Richard Jones studied and contributed much to understanding of the growth and metabolism of maize endosperm and embryos (Jones et al., 1984).
Effects of Global Climate Change (CO2 Increase) and Pollutants
Crop physiologists were a major force among early researchers who studied crop plant response to global climate change factors of elevated CO2 and temperature (Allen, 1994; Baker et al., 1995; Cure, 1985; Havelka et al., 1984a, 1984b; Kimball, 1983; Kimball et al., 1989; Lemon, 1983; Rogers et al., 1983; Reddy et al., 1995). Nearly all of this early work focused on effects of rising CO2, and provided solid information supporting previous observations. The only real surprise was that results from potted plants were found to show nonrealistically lower responses to CO2 and a "downregulation artifact" that was caused by root restriction as a function of decreased pot size (Thomas and Strain, 1991). Fortunately, many studies were done long-term in large pot or soil situations. Another feature learned regarded the existence of an acclimation effect of reduced photosynthetic capacity associated with decreased leaf N concentration, at least for C3 species (Bowes, 1993; Boote et al., 1997; Drake et al., 1997). This research on global climate change facilitated an early response of the scientific community to the policy debate of how global climate change would impact agricultural production and communities.
The past 50 yr has also seen the careful documenting of effects of environmental hazards such as ozone (Heagle, 1989; Allen, 1990; Unsworth et al., 1994), sulfur dioxide (Kropff, 1987), and ultraviolet irradiance (Caldwell and Flint, 1994).
Effects of Global Climate Change (Temperature Increase) and Normal Heat Stress
Nearly all of the initial global climate change work focused on effects of rising CO2. Effects of rising temperature have only been investigated well during the past 15 yr, although studies of short-term heat-stress episodes were studied and reviewed by Paulsen (1994). Studies of long-term elevated temperature showed that reproductive processes were adversely affected much sooner than were vegetative processes for rice (Oryza sativa L.; Baker and Allen, 1993; Baker et al., 1995), soybean [Glycine max (L.) Merr.; Boote et al., 2005; Pan, 1996], common bean (Phaseolus vulgaris L.; Prasad et al., 2002), peanut (Arachis hypogaea L.; Prasad et al., 2003), cotton (Gossypium hirsutum L.; Reddy et al., 1995, 2000), and sorghum [Sorghum bicolor (L.) Moench; Prasad et al., 2006]. These studies showed that 25°C was the typical optimum temperature for grain yield of rice, soybean, and peanut, and that yield declined progressively as temperature increased, causing complete failure at 35°C for rice and sorghum, and at 39 to 40°C for peanut and soybean (Boote et al., 2005). These findings highlighted that reproductive failures are an important problem if temperatures rise by 2 to 6°C during the next century, as projected by various global climate change scenarios. These findings for reproductive yield contrast dramatically from those of Idso et al. (1987), who found that increasing temperature increased CO2 responsiveness for strictly vegetative plants.
Effects of Environmental Factors on Yield
During the past 50 yr crop physiologists have gained a good understanding of the environmental effects of temperature, rainfall, solar radiation, and daylength on crop yield potential (Sinclair, 1994), along with discovering the genetic features of crop yield potential that enhanced assimilate capture along time and intensity of partitioning to yield (Duncan et al., 1978; Boote and Tollenaar, 1994; Evans, 1994). For example, they learned that whole-plant response is considerably conditioned by the rate of progress of the crop through its life cycle, that warm temperature was not always better for yield and that short days for a short-day plant were not optimum for yield. Rather, high yields are allowed by moderately cool temperature and somewhat nonoptimum daylength conditions that allowed the crop to progress slowly through the season (but to finish before frost), so as to maximize time for assimilate capture and time for assimilate partitioning to reproductive structures. This conclusion has been supported using experimental data and simulation studies with soybean (Spaeth et al., 1987), maize (Sinclair, 1994; Muchow et al., 1990) and wheat (Triticum spp.) (Sinclair and Bai, 1997).
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Improved Understanding of Crop Physiology: From First Principles to Holistic |
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TOPABSTRACTINTRODUCTIONTHE FULL CIRCLE OF...SIGNIFICANT DISCOVERIES OF CROP...Improved Understanding of Crop...THE PRESENT AND THE...REFERENCES |
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In the area of crop water relations, the theory and principles of crop water potential and hydraulics of water flow were studied and developed by many (Slatyer, 1969; Kramer, 1983; Boyer, 1969, 1976; Hsaio, 1973); however, by the early 1990s, crop physiologists discovered that there was more to crop water relations than simple hydraulics. Davies et al. (1990), Zhang and Davies (1990), Davies and Zhang (1991), and Tardieu et al. (1992) discovered that abscisic acid, produced by roots in drying soil regions and roots that encountered impedance stress or cold or nutrient deficit, served as a signal to reduce stomatal conductance and expansive processes, irrespective of hydraulic status of shoot tissue. About the same time, the role of the expansin enzymes in promoting or limiting cell wall elongation, again irrespective of good water relations, was described by Cosgrove (1999). The point is that there are multiple and redundant signals controlling plant response to water deficit, such that a researcher must be careful in studying single causes of tissue expansion, stomatal conductance, or photosynthesis (whether from primary hydraulics, growth regulators, or enzymatic proteins—the latter is certainly related to genetics).
Nitrogen is one of the most limiting nutrients, and photosynthetic response to N concentration or specific leaf N has been well described by a number of crop physiologists. But N effects on photosynthesis and productivity are considerably impacted by a number of second-order effects, such as shifts in root–shoot ratio (Boote, 1977; Kuiper et al., 1989), decreased hydraulic conductance to water (Radin and Boyer, 1982), N effects on leaf area expansion, N limitation on new sink strength, and carbohydrate feedback effects caused by lack of sink strength. Rapid increases in abscisic acid (Teplova et al., 1998; Mizrahi and Richmond, 1972) and decreases in cytokinin (Kuiper et al., 1989) in shoots were reported within 1–2 d after N deprivation. Kuiper et al. (1989) concluded that the shift in root–shoot ratio associated with N or P deficiency could be attributed to the plant growth regulators rather than the nutrient deficiency itself. Similarly, physiologists have described first-order effects of leaf photosynthesis response to leaf P as well as the mechanism by which P limitation in the chloroplast limits C flow from the chloroplast (Stitt, 1990), but again the same second-order effects such as shift in root–shoot ratio, hydraulic conductance of water (Radin and Eidenbock, 1984), P effect on new sink strength via lack of P for cell division and cell function, and carbohydrate feedback may be even more important. The point of these examples is to highlight that plants have redundant ways (including growth regulator signals) to control growth responses to water and nutrients such as N and P, and that crop physiologists are just now beginning to appreciate this complexity and redundancy of mechanisms of response.
The primary response of leaf photosynthesis to intercellular CO2 has been well characterized (Farquhar and Sharkey, 1982). However, the CO2 level itself has been shown to somehow signal for decreased N concentration (especially less Rubisco concentration), thus creating what has been called acclimation (Drake et al., 1997). Molecular genetics studies by Gesch et al. (2000) showed that a change in CO2, in 1 d, is sufficient to vary transcript abundance for the small subunit of Rubisco. Stitt's work (1990) highlighted the need to consider feedback effects of assimilate accumulation on photosynthesis via reduction in RuBP re-generation and Rubisco activase associated with orthophosphate availability/triose phosphate mechanisms, which is related to plant sink strength or ability to use the additional production of assimilate. To extend this story even further, the sink strength may be inadequate because the plant roots are confined in pots (Thomas and Strain, 1991) or because the plant temperature is low. Again, the conclusion is that there are multiple activities and levels to consider and there is a need to integrate to understand the full response of plants to CO2.
A singular focus on one process, one set of enzymes, or one set of genes, as the solution to an abiotic stress problem, will almost invariably fail. Improving or maintaining yield under field-level stresses must involve a multidisciplinary effort by physiologists and geneticists on the whole-plant level as well as tissue level of enzymes, metabolites, and genes.
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THE PRESENT AND THE FUTURE? A GENOCENTRIC ERA |
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TOPABSTRACTINTRODUCTIONTHE FULL CIRCLE OF...SIGNIFICANT DISCOVERIES OF CROP...Improved Understanding of Crop...THE PRESENT AND THE...REFERENCES |
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The second disconnect of genocentric research, according to Sinclair and Purcell (2005), has been to ignore the lessons of the past 40 yr of classical plant physiology research concerning the role of physiologically complex systems in altering whole-plant performance. Hageman, at the University of Illinois, for example, spent his entire career tracking down nitrate reductase, only to find that this single enzyme by itself had little impact on yield. In the other examples discussed above, regulation of plant systems is complex and there are considerable redundancies, such that alteration of a single process is compensated or damped out, giving little increase in plant growth or yield from modification of a single physiological process. Sinclair et al. (2004) gave a logical hypothetical example of how the damping process could occur from large increases in transcripts for Rubisco, to moderate increase in Rubisco, to less change in leaf-level photosynthesis, to much smaller increase in canopy assimilation, to even smaller increases successively in crop biomass and yield. Crop modeling efforts during the past 15 yr have illustrated abundantly well that genetic improvements come from integration and concurrent improvement in many traits and that the response to a given trait variation depends considerably on environment (Boote et al., 2001, 2003; Sinclair and Muchow, 2001).
What are future opportunities in crop physiology? We believe that molecular genetics is a fantastic tool for understanding physiology at the individual process level. Indeed, it seems molecular genetics is a much stronger tool for that purpose, than for the goal of genetic improvement of yield. It is this latter point that molecular genetic scientists seemed not to have gleaned from history. Our worry is that there will be belated recognition of the need for connection to whole-plant function, and evaluation of germplasm under normal field environments by whole-plant crop physiologists who can examine the integrated performance of the crop system. There is also a need for improved integration of all of these individual processes in crop simulation models, to be used for understanding the roles and interactions of all those specific genes and processes. This is not a role for the naïve, and there needs to be a wide-open-eyed skepticism about how well the processes may be represented in the models. While molecular geneticists have grand statistical classification tools, those tools do not lend themselves to quantitative analyses of yield outcomes of processes.
We conclude that crop physiology research, as reported by the many members of Division C-2 since its inception, has made a full circle, from emphasis on specific processes such as nitrate reductase, to whole-plant physiology, back to specific processes (genes to enzymes). We believe the present phase of the circle is in danger of losing focus on the whole-plant response. We also strongly suspect that the cycle will repeat itself, and that there will again be a recognition of the need to put together understanding of individual processes into a whole-plant perspective. The concern is that within a few years, most current whole-plant physiologists will be retired and not available for training students in this area, and few students are currently being trained in this area. We hope that the need for a whole-plant perspective is realized soon and there can be a ready capitalization on the physiological advances of the past 50 yr.
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TOPABSTRACTINTRODUCTIONTHE FULL CIRCLE OF...SIGNIFICANT DISCOVERIES OF CROP...Improved Understanding of Crop...THE PRESENT AND THE...REFERENCES |
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