Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome

C(4) photosynthesis is an evolutionary solution to high rates of photorespiration and low kinetic efficiency of Rubisco in CO(2)-depleted atmospheres of recent geologic time. About 7500 plant species are C(4), in contrast to 30 000 CAM and 250 000 C(3) species. All C(4) plants occur in approximately 90 genera from 18 angiosperm families. In all of these families, the C(4) pathway evolved independently. In many, multiple independent origins have occurred, such that over 30 distinct evolutionary origins of the C(4) pathway are recognized. Fossil and carbon isotope evidence show that the C(4) 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 C(4) plant evolution. All C(4) 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 CO(2) reduction and aridification. During the period of diversification, numerous traits arose in the C(3) flora that enhanced their performance in arid environments and atmospheres of reduced CO(2). Some of these traits may have predisposed certain taxa to develop the C(4) pathway once atmospheric CO(2) levels declined to a point where the ability to concentrate CO, had a selective advantage. Leading traits in C(3) plants that may have facilitated the initial transition to C(4) 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 C(3)-dominated woodlands into open, high-light habitats where herbaceous C(4) plants could succeed. Disturbances in the form of fire, and browsing by large mammals, increase during the time of C(4) plant evolution and diversification. Fire increased because of the drying climate, while browsing increased with the evolutionary diversification of the mammalian mega-fauna in the Oligocene and Miocene epochs. In summary, the origin of C(4) 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 C(4) plant evolution.