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Review
. 2004 Feb;161(2):341-370.
doi: 10.1111/j.1469-8137.2004.00974.x.

The evolution of C4 photosynthesis

Rowan F Sage  1
Affiliations
Free article
Review

The evolution of C4 photosynthesis

Rowan F Sage. New Phytol. 2004 Feb.
Free article

Abstract

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. Contents Summary 341 I. Introduction 342 II. What is C4 photosynthesis? 343 III. Why did C4 photosynthesis evolve? 347 IV. Evolutionary lineages of C4 photosynthesis 348 V. Where did C4 photosynthesis evolve? 350 VI. How did C4 photosynthesis evolve? 352 VII. Molecular evolution of C4 photosynthesis 361 VIII. When did C4 photosynthesis evolve 362 IX. The rise of C4 photosynthesis in relation to climate and CO2 363 X. Final thoughts: the future evolution of C4 photosynthesis 365 Acknowledgements 365 References 365.

Keywords: C3-C4 photosynthesis; Flaveria; carbon concentration; macroevolution; photorespiration; photosynthesis.

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