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Review Blackwell Publishing, Ltd. Tansley review The evolution of C4 photosynthesis Author for correspondence: Rowan F. Sage Rowan F. Sage Department of Botany, University of Toronto, 25 Willcocks Street, Toronto, Ontario M5S 3B2, Canada Tel: +1 416 978 7660 Fax: +1 416 978 5878 Email: [email protected] Received: 3 July 2003 Accepted: 16 October 2003 doi: 10.1046/j.1469-8137.2004.00974.x Contents Summary 341 VII. Molecular evolution of C4 photosynthesis 361 I. Introduction 342 VIII. When did C4 photosynthesis evolve 362 II. What is C4 photosynthesis? 343 IX. The rise of C4 photosynthesis in relation to climate and CO2 363 III. Why did C4 photosynthesis evolve? 347 X. Final thoughts: the future evolution of C4 IV. Evolutionary lineages of C4 photosynthesis 348 photosynthesis 365 V. Where did C4 photosynthesis evolve? 350 Acknowledgements 365 VI. How did C4 photosynthesis evolve? 352 References 365 Summary Key words: carbon concentration, C3–C4 C4 photosynthesis is a series of anatomical and biochemical modifications that con- photosynthesis, Flaveria, centrate CO2 around the carboxylating enzyme Rubisco, thereby increasing photo- macroevolution, photorespiration, synthetic efficiency in conditions promoting high rates of photorespiration. The C4 photosynthesis. pathway independently evolved over 45 times in 19 families of angiosperms, and thus represents one of the most convergent of evolutionary phenomena. Most origins of C4 photosynthesis occurred in the dicots, with at least 30 lineages. C4 photosynthesis first arose in grasses, probably during the Oligocene epoch (24–35 million yr ago). The earliest C4 dicots are likely members of the Chenopodiaceae dating back 15–21 million yr; however, most C4 dicot lineages are estimated to have appeared relatively recently, perhaps less than 5 million yr ago. C4 photosynthesis in the dicots originated in arid regions of low latitude, implicating combined effects of heat, drought and/or salinity as important conditions promoting C4 evolution. Low atmospheric CO2 is a significant contributing factor, because it is required for high rates of photorespiration. Consistently, the appearance of C4 plants in the evolutionary record coincides with periods of increasing global aridification and declining atmospheric CO2. Gene duplication followed by neo- and nonfunctionalization are the leading mechanisms for creating C4 genomes, with selection for carbon conservation traits under conditions promoting high photo- respiration being the ultimate factor behind the origin of C4 photosynthesis. © New Phytologist (2004) 161: 341–370 www.newphytologist.org 341 342 Review Tansley review Abbreviations CA, carbonic anhydrase; GDC, glycine decarboxylase; PCA, photosynthetic carbon assimilation; PCR, photosynthetic carbon reduction; PEPCase, phosphoenolpyru- vate carboxylase; PG, phosphogylcolate; PPDK, pyruvate orthophosphate dikinase; Rubisco, ribulose-1,5-bisphosphate carboxylase oxygenase; WUE, water-use efficiency. © New Phytologist (2004) 161: 341–370 of the primary productivity on the planet, and a large fraction I. Introduction of the primary production humans consume – either directly C4 photosynthesis is a series of biochemical and anatomical as plant material or indirectly via animal products – is derived modifications that concentrate CO2 around the carboxylating from C4 crops and pasture grasses (Lloyd & Farquhar, 1994; enzyme Rubisco. Many variations of C4 photosynthesis exist, Brown, 1999). C4 grasses and sedges dominate nearly all grass- reflecting at least 45 independent origins in 19 families of higher lands in the tropics, subtropics and warm temperate zones, and plants. C4 photosynthesis is present in about 7500 species of are major representatives of arid landscapes from the temperate flowering plants, or some 3% of the estimated 250 000 land zones to the tropics (Archibold, 1995; Sage et al., 1999b). Because plant species (Sage et al., 1999a). Most C4 plants are grasses of enhanced water and nutrient-use efficiency, C4 plants are (4500 species), followed by sedges (1500 species) and dicots also capable of growing in habitats that may be too harsh for (1200 species). C4 photosynthesis contributes about a quarter C3 species, such as rock outcrops (Fig. 1) and hypersaline or Fig. 1 C4 photosynthesis allows plants to grow in habitats that may otherwise be too harsh, as indicated by this C4 Muhlenbergia sp. growing on a rock face in Zion National Park, Utah, USA. Photo by R.F.S. www.newphytologist.org © New Phytologist (2004) 161: 341–370 Tansley review Review 343 arid soils of low latitude (Schulze et al., 1996). As a result, phosphoenolpyruvate carboxylase (PEPCase) and other existing complex ecosystems existed where there may otherwise have enzymes to concentrate CO2 around Rubisco (Fig. 2). In all been bare ground. versions of C4 photosynthesis, the initial step is the fixation of In recent years there has been widespread interest in the inorganic carbon by PEPCase, followed by the movement of the evolutionary diversification of C4 plants. Geologists are inter- resulting four-carbon acids to an interior compartment where ested because C4 photosynthesis affects atmosphere, climate Rubisco is localized (Hatch, 1987; Kanai & Edwards, 1999). and biotic systems through geological time (Lloyd & Here, CO2 is released by the decarboxylation of the four carbon Farquhar, 1994; Cerling et al., 1997; Pagani et al., 1999; Royer acid, and its concentration rises to a level that nearly saturates et al., 2001; Ehleringer et al., 2004). Zoologists and anthro- the Rubisco active site (von Caemmerer, 2000). The decarboxyla- pologists care because C4 plants influenced the evolution of tion reaction also produces a three-carbon acid, which diffuses mammals and hominids (MacFadden, 1997; van der Merwe back to the compartment where PEP carboxylase is located. If & Tschauner, 1999; Harris & Cerling, 2002; Janis et al., necessary, the three-carbon acid is converted to pyruvate, 2002). C4 crops and weeds have also affected historical trends, which is then phosphorylated to regenerate PEP. as shown by the rise of Mesoamerican civilizations based on While all C4 plants share a common theme, the specific maize, and the expansion of the transatlantic slave trade based means by which CO2 concentration occurs can vary sub- on cane sugar (Hobhouse, 1999; van der Merwe & Tschauner, stantially between the different evolutionary lineages (Edwards 1999). In the future, human-induced global change will favor & Walker, 1983; Kanai & Edwards, 1999). The only enzymatic widespread expansion of C4 grasslands at the expense of step common to all versions of C4 photosynthesis is the initial forests (Sage & Kubien, 2003). Climatologists and policy carboxylation reaction catalyzed by PEP carboxylase to yield makers are taking note because C4 grassland expansion alters oxaloacetic acid (OAA). Three decarboxylation enzymes regional climate and reduces air quality and biodiversity via (NADP-malic enzyme, NAD-malic enzyme and PEP carbox- effects on fire cycles and surface albedo. Finally, as a convergent ykinase) have been identified, and their relative abundance is phenomenon C4 photosynthesis is an excellent model for the basis for naming the three biochemical subtypes of C4 complex trait evolution in response to environmental change photosynthesis. If NADP-malic enzyme is used, OAA is con- (Monson, 2003). verted to malate which then diffuses to the interior compart- Given the significance of C4 plants, it is important to ment (Fig. 2). Pyruvate is formed during the decarboxylation understand the evolution of the C4 pathway. Much of what reaction, and this returns to the outer compartment to be we know about C4 photosynthesis was discovered in a 15 yr phosphorylated back to PEP. If NAD-ME is used, OAA is burst of research that followed the discovery of the pathway in transaminated to asparatate which then diffuses to the interior the mid-1960s (Edwards & Walker, 1983; Osmond, 1997; compartment (Fig. 2). Pyruvate is also formed during the Hatch, 1999). By the 1980s, the main features of the pathway NAD-ME decarboxylation reaction, but this is transaminated were identified, its taxonomic distribution described, and the to alanine, which then returns to the outer compartment ecological importance understood (Edwards & Walker, 1983). where it is converted to pyruvate and phosphorylated to yield Since then there has been substantial accumulation of infor- PEP. P EP carboxykinase-type plants form PEP during the mation from numerous disciplines, such that we can now pro- decarboxylation reaction, and this can return directly to the pose plausible hypotheses about the mechanisms, timing and outer compartment for carboxylation by PEPCase (Leegood environmental imperatives of C4 plant evolution. In this review, & Walker, 1999). I synthesize the current understanding of C4 plant biology Anatomically, C4 photosynthesis requires the modification to provide a comprehensive overview of the evolution of the of C3 leaf structure to form the inner compartment where C4 pathway. I begin by reviewing the characteristics that Rubisco is localized and CO2 can be concentrated (Dengler & define C4 photosynthesis, which is necessary both for back- Nelson, 1999). In most C4 plants this results in the formation ground review and to update our concepts in light of recent of a wreath-like cell arrangement, termed Kranz anatomy discoveries of single-celled patterns of C4 photosynthesis. (Fig. 2). In the textbook pattern of Kranz anatomy an outer I then address in turn four commonly