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

Abstract

C4 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 C4 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 C4 lineages in eudicots. The oldest chenopod C4 lineage dates back to the Eocene/Oligocene boundary, representing one of the first origins of C4 in plants, but still corresponding with the Oligocene decline of atmospheric CO2. In contrast to grasses, the rate of transitions from C3 to C4 is highest in ancestrally drought resistant (salt-tolerant and succulent) lineages, implying that adaptation to dry or saline habitats promoted the evolution of C4; and possible reversions from C4 to C3 are apparent. We conclude that the paradigm established in grasses must be regarded as just one aspect of a more complex system of C4 evolution in plants in general. © 2012 The Royal Society.