Continued adaptation of C4 photosynthesis after an initial burst of changes in the Andropogoneae grasses

C4 photosynthesis is a complex trait that sustains fast growth and high
productivity in tropical and subtropical conditions and evolved repeatedly
in flowering plants. One of the major C4 lineages is Andropogoneae, a
group of ~ 1,200 grass species that includes some of the world's most
important crops and species dominating tropical and some temperate
grasslands. Previous efforts to understand C4 evolution in the group have
compared a few model C4 plants to distantly related C3 species, so that
changes directly responsible for the transition to C4 could not be
distinguished from those that preceded or followed it. In this study, we
analyse the genomes of 66 grass species, capturing the earliest
diversification within Andropogoneae as well as their C3 relatives.
Phylogenomics combined with molecular dating and analyses of protein
evolution show that many changes linked to the evolution of C4
photosynthesis in Andropogoneae happened in the Early Miocene, between 21
and 18 Ma, after the split from its C3 sister lineage, and before the
diversification of the group. This initial burst of changes was followed
by an extended period of modifications to leaf anatomy and biochemistry
during the diversification of Andropogoneae, so that a single C4 origin
gave birth to a diversity of C4 phenotypes during 18 million years of
speciation events and migration across geographic and ecological spaces.
Our comprehensive approach and broad sampling of the diversity in the
group reveals that one key transition can lead to a plethora of phenotypes
following sustained adaptation of the ancestral state.