Anatomical enablers and the evolution of C_4 photosynthesis in grasses

摘要

C_4 photosynthesis is a series of anatomical and biochemical modifications to the typical C_3 pathway that increases the productivity of plants in warm, sunny, and dry conditions. Despite its complexity, it evolved more than 62 times independently in flowering plants. However, C_4 origins are absent from most plant lineages and clustered in others, suggesting that some characteristics increase C_4 evolvability in certain phylogenetic groups. The C_4 trait has evolved 22-24 times in grasses, and all origins occurred within the PACMAD clade, whereas the similarly sized BEP clade contains only C_3 taxa. Here, multiple foliar anatomy traits of 157 species from both BEP and PACMAD clades are quantified and analyzed in a phylogenetic framework. Statistical modeling indicates that C_4 evolvability strongly increases when the proportion of vascular bundle sheath (BS) tissue is higher than 15%, which results from a combination of short distance between BS and large BS cells. A reduction in the distance between BS occurred before the split of the BEP and PACMAD clades, but a decrease in BS cell size later occurred in BEP taxa. Therefore, when environmental changes promoted C_4 evolution, suitable anatomy was present only in members of the PACMAD clade, explaining the clustering of C_4 origins in this lineage. These results show that key alterations of foliar anatomy occurring in a C_3 context and preceding the emergence of the C_4 syndrome by millions of years facilitated the repeated evolution of one of the most successful physiological innovations in angiosperm history.