BIOLOGICAL PERSPECTIVES ON THE RISE OF C4 PHOTOSYNTHESIS

C4 photosynthesis is an evolutionary solution to high rates of photorespiration and low photosynthetic efficiency caused by high temperature and low atmospheric CO2. The C4 pathway evolved independently over 45 times in 19 families of angiosperms, and thus represents one of the most convergent of evolutionary phenomena. C4 photosynthesis is restricted to advanced angiosperm taxa that largely diversified in the past 40 million years, indicating the rise of advanced angiosperms is an important precondition for C4 evolution. C4 photosynthesis probably first arose in grasses during the Oligocene epoch. The earliest C4 dicots are Chenopodiaceae species present 15 to 21 million years ago; however, most C4 dicot lineages are estimated to have appeared in the past 5 million years. Recent C4 lineages provide insights into the environmental imperatives favoring C4 evolution, because the C4 ancestors and C3-C4 intermediate species still exist. C4 photosynthesis in recent dicot lineages originated in arid regions of low latitude, implicating combined effects of heat, drought and/or salinity as important conditions promoting the origin of C4 plants. Low atmospheric CO2 is a significant contributing factor for C4 evolution, because it is required for high rates of photorespiration. Consistently, the diversification of C4 plants in the evolutionary record coincides with a periods of increasing global aridification and declining atmospheric CO2. Aridification is thought to have promoted drought-adaptations in the C3 progenitors of the C4 lineages, such as enlarged bundle sheath cells, increased vein density, and an herbaceous life form. These adaptations likely predisposed certain taxa to evolve the C4 pathway by facilitating selection for C4-like carbon conservation mechanisms in low CO2 conditions. Aridity also promoted ecological factors favoring C4 species, namely fire, which removed woody C3 species and perpetuated hot, high-light conditions that favor C4 traits. Taken together, the mid-Cenozoic appears to be the first time in earth’s history when physical (aridification and low CO2) and biological factors (advanced herbaceous angiosperms) combined to create the conditions allowing for the rise of C4 photosynthesis.