The evolution of C4 photosynthesis

C-4 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 C-4 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 C-4 photosynthesis occurred in the dicots, with at least 30 lineages. C-4 photosynthesis first arose in grasses, probably during the Oligocene epoch (24-35 million yr ago). The earliest C-4 dicots are likely members of the Chenopodiaceae dating back 15-21 million yr; however, most C-4 dicot lineages are estimated to have appeared relatively recently, perhaps less than 5 million yr ago. C-4 photosynthesis in the dicots originated in arid regions of low latitude, implicating combined effects of heat, drought and/or salinity as important conditions promoting C-4 evolution. Low atmospheric CO2 is a significant contributing factor, because it is required for high rates of photorespiration. Consistently, the appearance of C-4 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 C-4 genomes, with selection for carbon conservation traits under conditions promoting high photorespiration being the ultimate factor behind the origin of C-4 photosynthesis.