Faster relaxation of nonphotochemical quenching in C4 than in C3 species.

Acceleration of photoprotective nonphotochemical quenching (NPQ) responses to changes in light intensity has been suggested as a strategy to enhance crop yield. Our current understanding of NPQ overwhelmingly comes from C3 species, and despite many key crops being C4, separating the impact of photosynthetic pathway from species-specific effects is complicated by the large evolutionary distance between most C3 and C4 species. By conducting a series of experiments on C3 and C4 species from Alloteropsis, Flaveria, and Cleome, genera which encompass both pathways, we controlled for phylogenetic distance and showed that NPQ relaxation is significantly faster in C4 than in C3 species. This trend is supported further by a meta-analysis compiling NPQ data on C3 and C4 species from intraspecific published studies and new measurements. Analysis of dynamic NPQ responses in C3 and C4 leaves infiltrated with inhibitors revealed that faster relaxation observed in C4 species is driven by a greater contribution of energy-dependent quenching (qE) to overall NPQ. This C4-associated enhancement of qE in turn is linked to altered regulation of lumen pH in C4 species, reflecting increases in cyclic electron flow and membrane proton conductivity to meet the increased adenosine triphosphate (ATP) demands of the C4 pathway. Altogether, our results indicate that NPQ responses in C4 species may already be optimized to maintain high photosynthetic efficiency in fluctuating light conditions. Given the intrinsically faster NPQ in C4 photosynthesis, further acceleration of NPQ may have limited scope to enhance crop photosynthetic efficiency.