The evolution of C₄photosynthesis

Abstract

Contents Summary 341 Introduction 342 What is C4 photosynthesis? 343 Why did C4 photosynthesis evolve? 347 Evolutionary lineages of C4 photosynthesis 348 Where did C4 photosynthesis evolve? 350 How did C4 photosynthesis evolve? 352 Molecular evolution of C4 photosynthesis 361 When did C4 photosynthesis evolve 362 The rise of C4 photosynthesis in relation to climate and CO2 363 Final thoughts: the future evolution of C4 photosynthesis 365 Acknowledgements 365 References 365 Summary C4 photosynthesis is a series of anatomical and biochemical modifications that concentrate CO2 around the carboxylating enzyme Rubisco, thereby increasing photosynthetic efficiency in conditions promoting high rates of photorespiration. The C4 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 photorespiration being the ultimate factor behind the origin of C4 photosynthesis.

Leaf plasticity in successive selection cycles of 'Saracura' maize in response to periodic soil flooding

“…Studies on parallel vascular bundles in grasses showed that C4-type species present smaller distance between the vascular bundles than C3 type (Ueno et al, 2006). Such characteristic, present in C4-type plants, conveys higher ability in photosynthate translocation and higher water distribution in environments with water restriction and high temperatures (Sage, 2004). Just as a greater phloem thickness could increase the photosynthetic flow, a reduced space between the vascular bundles in the selection cycles of 'Saracura' maize could also increase this flow, because it would promote higher photosynthate distribution (Roth-Nebelsick et al, 2001) in addition to a higher water distribution.…”

The potential of planets orbiting red dwarf stars to support oxygenic photosynthesis and complex life

“…In the majority of C3 plants, oxygen reduces CO 2 fixation by some 25% (see e.g. Lambers et al, 1998 andSage 2003, for a full discussion).…”

Phylogenetic signals in the realized climate niches of Chinese grasses (Poaceae)

“…Many studies addressing climatic effects on C 4 grass distribution (Teeri and Stowe 1976;Chazdon 1978;Vogel and Fuls 1978;Rundel 1980;Hattersley 1983;Collins and Jones 1985;Klink and Joly 1989;Paruelo and Lauenroth 1996;P'yankov et al 2000) reported the positive correlation between growing season temperature and C 4 grass abundance. Whereas precipitation gradients seemed to have less impact on C 3 and C 4 grass distribution globally (Sage 2004).…”

“…In C 3 photosynthesis, CO 2 is directly fixed by the oxygen sensitive ribulose-bis-phosphate carboxylase/oxygenase (Rubisco) and the first stable fixation product is the C 3 compound phosphoglyceric acid (PGA). In C 4 photosynthesis, CO 2 is initially fixed by the oxygeninsensitive phosphoenolpyruvate carboxylase (PEPC) and the first stable fixation product is the C 4 compound, malic acid (Sage 2004). C 4 photosynthesis is a major evolutionary success and about of the species in the grass family utilize this pathway.…”

“…C 4 photosynthesis is a major evolutionary success and about of the species in the grass family utilize this pathway. The grass family is economically and ecologically important, accounting for about 25% of global gross primary productivity (Sage 2004;Edwards et al 2010) and about 23% of global grain production (Monfreda et al 2008). Grasses utilizing the C 4 photosynthetic pathway dominate nearly all grasslands in tropical, subtropical, and warm temperate zones, and rank among the world's most important crops, weed plants, and potential biofuels such as corn, sugarcane, and sorghum (Sage et al 1999a).…”