Up-regulation of bundle sheath electron transport capacity under limiting light in C4 Setaria viridis

Abstract

C4 photosynthesis is a biochemical pathway that operates across mesophyll and bundle sheath (BS) cells to increase CO2 concentration at the site of CO2 fixation. C4 plants benefit from high irradiance but their efficiency decreases under shade causing a loss of productivity in crop canopies. We investigated shade acclimation responses of a model NADP-ME monocot Setaria viridis focussing on cell-specific electron transport capacity. Plants grown under low light (LL) maintained CO2 assimilation rates similar to high light plants but had an increased chlorophyll and light-harvesting-protein content, predominantly in BS cells. Photosystem II (PSII) protein abundance, oxygen-evolving activity and the PSII/PSI ratio all increased in LL BS cells indicating a higher capacity for linear electron flow. PSI, ATP synthase, Cytochrome b6f and the chloroplastic NAD(P) dehydrogenase complex, which constitute the BS cyclic electron flow machinery, were all upregulated in LL plants. A decline in PEP carboxylase activity in mesophyll cells and a consequent shortage of reducing power in BS chloroplasts was associated with the more oxidised redox state of the plastoquinone pool in LL plants and the formation of PSII - light-harvesting complex II supercomplexes with an increased oxygen evolution rate. Our results provide evidence of a redox regulation of the supramolecular composition of Photosystem II in BS cells in response to shading. This newly identified link contributes to understanding the regulation of PSII activity in C4 plants and will support strategies for crop improvement including the engineering of C4 photosynthesis into C3 plants. Significance statementThe efficiency of C4 photosynthesis decreases under low irradiance causing a loss of productivity in crop canopies. We investigate shade acclimation of a model NADP-ME monocot, analysing cell-specific protein expression and electron transport capacity. We propose a regulatory pathway controlling abundance and activity of Photosystem II in bundle sheath cells in response to irradiance.