A broader model for C4 photosynthesis evolution in plants inferred from the goosefoot family (Chenopodiaceae s.s.)

C(4) photosynthesis is a fascinating example of parallel evolution of a complex trait involving multiple genetic, biochemical and anatomical changes. It is seen as an adaptation to deleteriously high levels of photorespiration. The current scenario for C(4) evolution inferred from grasses is that it originated subsequent to the Oligocene decline in CO(2) levels, is promoted in open habitats, acts as a pre-adaptation to drought resistance, and, once gained, is not subsequently lost. We test the generality of these hypotheses using a dated phylogeny of Amaranthaceae s.l. (including Chenopodiaceae), which includes the largest number of C(4) lineages in eudicots. The oldest chenopod C(4) lineage dates back to the Eocene/Oligocene boundary, representing one of the first origins of C(4) in plants, but still corresponding with the Oligocene decline of atmospheric CO(2). In contrast to grasses, the rate of transitions from C(3) to C(4) is highest in ancestrally drought resistant (salt-tolerant and succulent) lineages, implying that adaptation to dry or saline habitats promoted the evolution of C(4); and possible reversions from C(4) to C(3) are apparent. We conclude that the paradigm established in grasses must be regarded as just one aspect of a more complex system of C(4) evolution in plants in general