New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins

Abstract

Summary: Grasses rank among the world’s most ecologically and economically important plants. Repeated evolution of the C 4 syndrome has made photosynthesis highly efficient in many grasses, inspiring intensive efforts to engineer the pathway into C 3 crops. However, comparative biology has been of limited use to this endeavor because of uncertainty in the number and phylogenetic placement of C 4 origins. We built the most comprehensive and robust molecular phylogeny for grasses to date, expanding sampling efforts of a previous working group from 62 to 531 taxa, emphasizing the C 4‐rich PACMAD (Panicoideae, Arundinoideae, Chloridoideae, Micrairoideae, Aristidoideae and Danthonioideae) clade. Our final matrix comprises c. 5700 bp and is > 93% complete. For the first time, we present strong support for relationships among all the major grass lineages. Several new C 4 lineages are identified, and previously inferred origins confirmed. C 3/C 4 evolutionary transitions have been highly asymmetrical, with 22–24 inferred origins of the C 4 pathway and only one potential reversal. Our backbone tree clarifies major outstanding systematic questions and highlights C 3 and C 4 sister taxa for comparative studies. Two lineages have emerged as hotbeds of C 4 evolution. Future work in these lineages will be instrumental in understanding the evolution of this complex trait.