A broader model for C 4 photosynthesis evolution in plants inferred from the goosefoot family (Chenopodiaceae s.s.)

Abstract

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.