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Carnegie Institution of Washington, Department of Plant Biology Stanford, California 94305
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INTRODUCTION |
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 TOP INTRODUCTION LITERATURE CITED |
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8000 of 250 000), their economic and ecological importance, particularly in the tropics, is disproportionately large. This volume, C4 Plant Biology edited by Rowan F. Sage and Russell K. Monson, is a testament to that importance and its impact on fields as diverse as plant physiology, ecology, geology, and anthropology, to name a few. Indeed, readers from the entire spectrum of plant biology are likely to find at least a few chapters of interest in this book, which is divided into five sections on various aspects of C4 plant biology: perspectives, structure–function, ecology, evolution, and human interactions. The perspectives section contains an excellent chapter by Sage on the evolutionary constraints that were likely important drivers in the evolution of this pathway. The other chapter in this section, a historical overview by Marshall Hatch, reviews the events and key players in the discovery of C4 photosynthesis. Hatch also provides a context for much of the subsequent biochemical research into the pathway he helped elucidate in the 1960s. Some of the individuals he cites for their key roles also contributed chapters to this volume. The structure–function section focuses on the biochemical and morphological features of the C4 syndrome. Gerald Edwards, one of the workers highlighted by Hatch, co-authored a chapter with Ryuzi Kanai on the biochemistry of C4 photosynthesis. They describe the biochemical workings that underpin the whole-plant responses to CO2, light, and temperature, which play a central role in the book's subsequent chapters on the ecology of C4 plants. Readers who are not expert in the details of C4 photosynthesis should start here, as a careful reading will enhance an understanding of the concepts advanced in later chapters. Other chapters in this section address regulation of the pathway (Leegood and Walker), leaf structure and development (Dengler and Nelson), and modeling C4 photosynthesis. The last chapter, by Suzanne von Caemmerer and Robert Furbank, is a nice summary of the key aspects of this pathway and how they can be captured in a small set of equations. Though much of the material in this section of the book concerns topics that were generally understood by about 1980, all of the chapters effectively integrate older and newer information, establishing a strong background for the book's other sections.
The next section of the book concerns the ecology of C4 photosynthesis, in particular how the biochemical and anatomical adaptations of this pathway influence plant performance in the environment. A chapter by Steve Long discusses the factors that influence how the biochemical differences between C3 and C4 plants translate to the whole-plant level. Long competently and clearly tackles the task of describing how the higher resource use efficiencies (water, nitrogen, light) conferred by the C4 pathway are modulated by environmental factors like water and nutrient limitations. Long also addresses the puzzling issue of whether there exists some fundamental ‘flaw’ in the operation of C4 photosynthesis in cold temperatures, as has been suggested due to the scarcity of these plants in colder climates. While the advantage of C4 relative to C3 photosynthesis due to elimination of photorespiration decreases as temperature decreases, this does not imply that there should be no C4 plants in very cold climates. Long, who has done some of the seminal work on C4 responses to low temperature, first reviews some of the proposed reasons for C4 impairment at low temperatures. Then he discusses the genus Miscanthus, which contains several species found at high altitudes in Taiwan and Japan, as evidence that there is no inherent flaw in the operation of the C4 syndrome at low temperatures.
The following chapter by Alan Knapp and Ernesto Medina compares two New World ecosystems that are dominated by C4 plants, the tropical savannah of South America and the temperate grassland of North America. One refreshing aspect of this chapter is a discussion of the external factors (e.g., fire, grazing) that influence the success of C4 plants in the field, in addition to the biochemical factors previously discussed. In the next chapter, Sage, Wedin, and Li appeal to these biochemical arguments when they advance mechanisms that explain the observed distribution of C3 and C4 plants, but they also discuss other kinds of ecological factors that influence the distribution of these photosynthetic types (e.g., grassland–woodland interactions). One of the more interesting parts of this chapter discusses the future distribution and abundance of C4 plants. As Sage et al. point out, several of the ongoing global changes humans are inflicting on the planet should benefit C3 plants at the expense of C4 plants (e.g., rising CO2 levels, increasing nitrogen deposition, suppression of fire cycles). Others are likely to benefit C4 plants more (conversion of tropical forests to grasslands, hotter summers). Of course, many if not all of these factors will interact, making predictions of future distributions very difficult. This is likely to be a hot topic of research among ecologists, biogeographers, and biogeochemists for years to come.
A chapter by Heckathorn, McNaughton, and Coleman offers an intriguing discussion of the interactions between herbivores and C4 plants. While the generally lower nitrogen and higher fiber content of C4 foliage should be less appealing to herbivores than C3 leaf tissue, Heckathorn et al. argue that the evidence for herbivore preference for C3 plants is inconclusive. Indeed, C4-dominated ecosystems are characterized by a greater degree of herbivory than are C3-dominated ecosystems. Heckathorn et al. claim that factors other than leaf quality (like a greater ability to withstand high levels of folivory) can explain this pattern. They also hypothesize that these differences may help explain the structure and composition of herbivore groups in different ecosystems. A recent paper by Magnusson et al. (1999)
provides some support for this argument. These workers studied the contributions of C3 and C4 plants in an Amazonian savanna to higher trophic levels by analyzing the carbon isotope composition of food plants and animals from different heterotrophic groups. They found that endothermic vertebrates preferred C3-based food chains, while ectothermic vertebrates obtained most of their carbon from C4 grasses.
While the ecology section synthesizes much interesting material, key questions are incompletely resolved. The chapters by Long, Knapp, and Medina and Sage et al. are refreshingly open about the fact that photosynthesis, growth, and ecological success are often loosely connected. Still, it is unclear exactly which aspects of the ecology and biogeography of C4 plants are controlled by the biochemistry and physiology of the C4 photosynthesis pathway and which are controlled by other characteristics of these plants. Some of the ecological successes and limitations of C4 plants are direct consequences of the C4 physiology, but others appear to be more related to historical or phylogenetic factors. One interesting example concerns the limited success of C4 species at low temperatures. Based on photosynthesis alone, C4 plants should be competitively superior across the entire temperature spectrum under full glacial CO2 concentrations. Coupled with the conclusion that there is no fundamental problem limiting the C4 pathway at cold temperatures, this leads to a conundrum. What limited C4 species during full glacial conditions? Or why aren't C4 plants able to colonize present-day higher elevation environments in greater numbers, where the lower partial pressures of CO2 should favor them over C3 plants? The most likely explanation for these questions is that factors other than photosynthesis ultimately explain the temperature sensitivity of C4 plants.
Another intriguing example of the interface between C4 photosynthesis and other features of the plants with this pathway concerns the rarity of C4 trees. Based on the physiology of photosynthesis, C4 species should be successful in many tropical habitats that support trees. It is easy to see why a C4 grass might be a poor competitor against any tree, but it is less clear why there are extremely few C4 trees in these habitats. One interesting possibility, discussed in the chapter by Monson, is that the limiting factor is potential to allocate new biomass to leaf area. Another is that the C4 pathway makes plants intrinsically less competent to use light energy in sunflecks. Finally, C4 might be rare in trees simply because of time. C4 trees should be strong competitors under full-glacial CO2, but they might be quite CO2-sensitive. Perhaps the time windows with low CO2 simply have not been long enough for the broad emergence of C4 trees. While the book does not resolve these and a number of other similar issues, several chapters present what is known and present possibilities that are interesting, if difficult to verify.
The section of the book that explores the evolution of C4 photosynthesis integrates many of the concepts discussed in the biochemistry and ecology sections. The chapter by Monson on the evolution of the C4 biochemistry focuses on a fascinating twist to the C4 story. While the earlier and later chapters consider the advantages and disadvantages of the full-blown C4 pathway, Monson tackles the question of initial advantage. The C4 pathway is biochemically and morphologically complex. It almost certainly did not evolve in a single step. But what progression of small changes could result in selection for each change, in the absence of the entire syndrome? With a perspective informed by both models and studies with C3-C4 intermediates, Monson outlines a feasible scenario. Finding a conclusive test for this hypothesis will be an intriguing challenge for the future.
Kellogg addresses the systematic component of the evolution of plants with the C4 photosynthesis pathway. Based on phylogenies for many groups with C4 taxa, she documents the frequent evolutionary origin of the syndrome and argues that C4 photosynthesis is a collection of related pathways, linked through the carboxylation of PEP and stabilized through the C4 morphology. Her evidence on multiple origins sharpens the questions on selection for the intermediates, while suggesting that their advantage must be substantial, to recur in so many taxa, over such a brief period. Thure Cerling broadens the treatment of time, by reviewing the paleoevidence for C4 photosynthesis. The observation that the oldest C4 plants occurred 6–8 million years before they became abundant anywhere is very intriguing. Did the C4 species begin to cover large regions of the earth as the C3 species were starved of CO2? Cerling's discussion of the trade-off between CO2 and water limitation potentially extends this hypothesis to a broad range of habitats in a drying, low-CO2 world. It will be fun to see future research connect these climatic factors with grazing, fire, and nutrients.
Cerling's discussion of the application of carbon isotope ratios to the question of C4 in past floras and past and present diets is useful but sobering. His clear treatment of the variability in the isotopic signature of C3 plants, plus effects due to variation in the isotopic composition of the air, plus additional challenges of aquatic measurements, establishes both the limitations and the potential of this important technique. Once the parameters are set, the approach of assessing C4 abundance through the isotopic composition of grazers cleverly reveals patterns that would be very obscure in the absence of isotopic information.
Two chapters on C4 plants and humanity provide fascinating twists on the evidence for the broad importance of the C4 pathway. The chapter by Brown points out the predominance of C4 plants in tropical agriculture and prevalence in many temperate crops. He also discusses the high incidence of this pathway among weedy species. The temporal correspondence between the expansion of the C4 pathway and the origin of the evolutionary branch that led to humans suggests a link. The chapter by van der Merwe and Tschauner explores this in detail, connecting the ecological and physiological factors that favor C4 with the shifts in social organization and behavior that accompanied the movement of the earliest hominids from the forest to the savanna. The suggestion that human culture owes its origin to C4 photosynthesis makes some sense, though I suspect readers will think of additional factors that may have played some role.
The theme of close interaction between biology and culture extends into van der Merwe and Tschauner's discussion of the origin of C4 crops. The evidence for long-distance transport of crop species, e.g., from China to Europe more than 3500 years ago, is startling. Think about farmers in classical Greece growing Chinese millets as an exotic cereal. But it is even more amazing to think about the hypothesis, discussed by van der Merwe and Tschauner, that several features of maize made it almost preadapted to drive societal stratification. Because maize is absent from nature, hard to grow, and potentially very productive, it could be used for the self-aggrandizement of those who knew the secrets of its cultivation.
The final chapter of the book, by Sage, Li, and Monson, provides a useful compendium of known C4 taxa and their taxonomic distribution among families and genera, as well as the biochemical subtypes and number of species within genera. Interestingly, just five plant families contain the vast majority of known C4 species, and Sage et al. use this fact to speculate on the habitat conditions that may have influenced where C4 plants first evolved.
While this volume effectively treats a broad range of topics, a few omissions are notable. One is the global-scale biogeography models that simulate past, present, and future distributions of C4 grasslands (e.g., Haxeltine and Prentice, 1996
). Another is the role of C4 photosynthesis in the global carbon cycle. Because C4 plants dominate several globally extensive ecosystems (e.g., savannahs, tropical grasslands, many temperate grasslands), they play an important role in the terrestrial carbon cycle. Model-based estimates of the proportion of global NPP due to C4 photosynthesis vary from 18% (Ehleringer, Cerling, and Helliker, 1997
) to as high as 30% (Berry, 1994
). These numbers partly reflect the very high production rates that can be achieved by these plants in hot climates. Indeed, in his chapter on environmental responses, Steve Long describes the unusual case of a C4 plant, Echinochloa polystachya, that forms extensive stands on the floodplains of the Amazon. In order to keep their upper leaves from being submerged by the rising floodwaters, these stands achieve phenomenal growth rates (over 100 tons of dry matter per hectare during the ten months of flooding!). While this example is clearly exceptional, it does illustrate the potential for high production that C4-dominated ecosystems can achieve when they are not limited by water or nutrients.
Perhaps even more important than the total production due to C4 plants is its variability on an interannual and seasonal basis. Because C4 plants typically thrive in arid or semi-arid regions or areas that experience periodic water shortages and/or temperature stress, they often experience conditions that alter their photosynthesis and respiration from one year to the next, or even within the course of a growing season. This is especially true in areas that experience climate anomalies that are strongly forced by the El Niño/La Niña (ENSO) cycle. An analysis of the correlation between Pacific SST (sea surface temperature) anomalies and NDVI (normalized difference vegetation index, a measure of vegetation density and vigor) anomalies demonstrates that many of these areas with strong correlations are savannahs and grasslands in South America, Africa, and Australia (Myneni, Los, and Tucker, 1996
). Determining the relative amounts of net carbon uptake among C3 ecosystems, C4 ecosystems, and the ocean will take on increasing importance as global changes like the increasing CO2 concentration and expected climate warming affect the global distribution of C3 and C4 plants.
It is a long way from the km of PEP-C (phosphoenolpyruvate carboxylase) to the emergence of an Incan elite. This volume covers the distance with chapters that are all clearly written and well integrated. Several cover topics where the basics have been worked out for many years. Others are quite speculative. A substantial fraction of the material is repeated, largely because issues like the oxygen sensitivity of Rubisco and resource use efficiency underlie many aspects of the biology of C4 plants. The book's contributors are unabashedly positive about C4 photosynthesis. But they clearly explain their enthusiasm. The book documents, beyond the shadow of a doubt, how and why C4 plants can be superior to C3 plants in a variety of natural and agronomic settings.
Maybe we were already members of the C4 fan club, but we now have a broader foundation for enthusiasm, except perhaps for the role of maize in leading to social inequality. That deserves some thought.
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FOOTNOTES |
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LITERATURE CITED |
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TOPINTRODUCTIONLITERATURE CITED |
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Ehleringer, J. R., T. E. Cerling, and B. R. Helliker. 1997 C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112:285–299.
Haxeltine, A. and I. C. Prentice. 1996 BIOME3: an equilibrium terrestrial biosphere model based on ecophysiological constraints, resource availability, and competition among plant functional types. Global Biogeochemical Cycles 10: 693–711.[CrossRef][ISI]
Magnusson, W. E., M. C. deArango, R. Cintra, A. P. Lima, L. A. Martinelli, T. M. Sanaiotto, H. L. Vasconcelos, and R. L. Victoria. 1999 Contributions of C3 and C4 plants to higher trophic levels in an Amazonian savanna. Oecologia 119:91–96.
Myneni, R. B., S. O. Los, and C. J. Tucker. 1996 Satellite-based identification of linked vegetation index and sea-surface temperature anomaly areas from 1982–1990 for Africa, Australia and South-America. Geophysical Research Letters 23(#7):729–732.
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