Promotion of cyclic electron transport around photosystem I during the evolution of NADP-malic enzyme-type C4 photosynthesis in the genus Flaveria

C-4 plants display higher cyclic electron transport activity than C-3 plants. This activity is suggested to be important for the production of ATPs required for C-4 metabolism. To understand the process by which photosystem I (PSI) cyclic electron transport was promoted during C-4 evolution, we conducted comparative analyses of the functionality of PSI cyclic electron transport among members of the genus Flaveria, which contains several C-3, C-3-C-4 intermediate, C-4-like and C-4 species. The abundance of NDH-H, a subunit of NADH dehydrogenase-like complex, increased markedly in bundle sheath cells with the activity of the C-4 cycle. By contrast, PROTON GRADIENT REGULATION5 (PGR5) and PGR5-LIKE1 increased in both mesophyll and bundle sheath cells in C-4-like Flaveria palmeri and C-4 species. Grana stacks were drastically reduced in bundle sheath chloroplasts of C-4-like F. palmeri and C-4 species; these species showed a marked increase in PSI cyclic electron transport activity. These results suggest that both the expression of proteins involved in PSI cyclic electron transport and changes in thylakoid structure contribute to the high activity of cyclic electron flow in NADP-malic enzyme-type C-4 photosynthesis. We propose that these changes were important for the establishment of C-4 photosynthesis from C-3-C-4 intermediate photosynthesis in Flaveria.