DLDG1, the Arabidopsis Homolog of the Cyanobacterial H⁺-Extrusion Protein, Regulates Non-Photochemical Quenching in Chloroplasts

Abstract

Abbreviations: CemA, Chloroplast envelop membrane protein A; Chl, chlorophyll; DLDG1, Day-length-dependent delayed-greening1; CYO1, Cotyledon-specific chloroplast biogenesis 2 factor1; ΔpH, H + gradient across the thylakoid membrane; ΔΨ, electric potential; EYFP, enhanced yellow fluorescent protein; FLAP1, Fluctuating-light acclimation protein1; GFP, green fluorescent protein; LHC, light-harvesting complexes; NPQ, non-photochemical quenching; PS, photosystem; pmf, proton motive force across the thylakoid membrane; PPFD, photosynthetic photon-flux density; PxcA, proton-extrusion-protein A; SFR2, Sensitive to freezing2; VDE, violaxanthin de-epoxidase. 3 Abstract Plants convert solar energy into chemical energy through photosynthesis, which supports almost all life activities on earth. Because the intensity and quality of sunlight can change dramatically throughout the day, various regulatory mechanisms help plants adjust their photosynthetic output accordingly, including the regulation of light energy accumulationto prevent the generation of damaging reactive oxygen species. Non-photochemical quenching (NPQ) is a regulatory mechanism that dissipates excess light energy, but how it is regulated is not fully elucidated. Herein, we report a new NPQ-regulatory protein named Day-Length-dependent Delayed-Greening1 (DLDG1). The Arabidopsis DLDG1 associates with the chloroplast envelope membrane, and the dldg1 mutant had a large NPQ value compared with wild type. The mutant also had a pale-green phenotype in developing leaves but only under continuous light; this phenotype was not observed when dldg1 was cultured in the dark for ≥8 h per day. DLDG1 is a homolog of the plasma-membrane-localizing cyanobacterial proton-extrusion-protein A that is required for light-induced H + extrusion, and also shows similarity in its amino-acid sequence to that of Ycf10 encoded in the plastid genome. Arabidopsis DLDG1 enhances the growth-retardation phenotype of the Escherichia coli K + /H + antiporter mutant, and the everted membrane vesicles of the E. coli expressing DLDG1 show the K + /H + antiport activity. Our findings suggest that DLDG1 functionally interacts with Ycf10 to control H + homeostasis in chloroplasts, which is important for the light-acclimation response, by optimizing the extent of NPQ.

Engineering Improved Photosynthesis in the Era of Synthetic Biology

“…Significant increases in growth rates were recently obtained in tobacco by accelerating recovery from photoprotection by means of an improved non-photochemical quenching (NPQ) ( Kromdijk et al., 2016 ). Furthermore, different recent approaches have emerged as alternatives to improve photosynthesis based on changes in NPQ ( Murchie and Niyogi, 2011 , Harada et al., 2019 ) as well as on the regulation of the cytochrome b 6 f complex and its related proteins PsbS and Rieske FeS subunit ( Shikanai, 2014 , Ermakova et al., 2019a ). Apart from the alterations in NPQ or cytochrome b 6 f complex, two main ideas suggested to optimize light-use efficiency (LUE) by plants are (1) the expansion of the light absorption spectrum to capture more of the available light and (2) the reduction of antenna size of the photosystems ( Terao and Katoh, 1996 , Ort et al., 2011 , Bielczynski et al., 2019 ).…”