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 CO2 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 CO2. 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.