Environmental and Evolutionary Preconditionsfor the Origin and Diversification of the C₄ PhotosyntheticSyndrome

Abstract: C4 photosynthesis is an evolutionary solution to high rates of photorespiration and low kinetic efficiency of Rubisco in CO2‐depleted atmospheres of recent geologic time. About 7500 plant species are C4, in contrast to 30 000 CAM and 250 000 C3 species. All C4 plants occur in approximately 90 genera from 18 angiosperm families. In all of these families, the C4 pathway evolved independently. In many, multiple independent origins have occurred, such that over 30 distinct evolutionary origins of the C4 pathway are recognized. Fossil and carbon isotope evidence show that the C4 syndrome is at least 12 to 15 million years old, although estimates based on molecular sequence comparisons indicate it is over 20 million years old. The evolutionary radiation of herbaceous angiosperms may have been required for C4 plant evolution. All C4 species occur in advanced angiosperm families that appeared in the fossil record in the past 70 million years. Most of these families diversified in terms of genera and species numbers between 20 to 40 million years ago, during a period of global cooling, atmospheric CO2 reduction and aridification. During the period of diversification, numerous traits arose in the C3 flora that enhanced their performance in arid environments and atmospheres of reduced CO2. Some of these traits may have predisposed certain taxa to develop the C4 pathway once atmospheric CO2 levels declined to a point where the ability to concentrate CO2 had a selective advantage. Leading traits in C3 plants that may have facilitated the initial transition to C4 photosynthesis include close vein spacing and an enlargement of the bundle sheath cell layer to form a Kranz‐like anatomy. Ecological factors not directly connected with photosynthesis probably also played a role. For example, extensive ecological disturbance may have been needed to convert C3‐dominated woodlands into open, high‐light habitats where herbaceous C4 plants could succeed. Disturbances in the form of fire, and browsing by large mammals, increase during the time of C4 plant evolution and diversification. Fire increased because of the drying climate, while browsing increased with the evolutionary diversification of the mammalian megafauna in the Oligocene and Miocene epochs. In summary, the origin of C4 plants is hypothesized to have resulted from a novel combination of environmental and phylogenetic developments that, for the first time, established the preconditions required for C4 plant evolution.

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