DAY-LENGTH-DEPENDENT DELAYED-GREENING1, the Arabidopsis Homolog of the Cyanobacterial H+-Extrusion Protein, Is Essential for Chloroplast pH Regulation and Optimization of Non-Photochemical Quenching

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 accumulation to 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. In this study, 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/d. 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.

Plastidial transporters KEA1 and KEA2 at the inner envelope membrane adjust stromal pH in the dark

“…In this respect it should be noted that AtKEA2 is localized to distinct spots on the envelope membrane and we previously suggested the protein could be part of the thylakoid biogenesis centers (Aranda-Sicilia et al, 2016). A direct relationship between thylakoid lumen pH and K + /H + activity at the envelope membrane was also recently proposed by Harada et al (2019), who characterized a new inner envelope protein, DLDG1, with K + /H + exchange activity in an E. coli inverted vesicle assay. Disruption of this protein caused a more sustained NPQ induction and significantly higher 9-AA accumulation in intact chloroplasts, indicative of an increased thylakoid membrane ΔpH.…”

“…A direct relationship between thylakoid lumen pH and K + /H + activity at the envelope membrane was also recently proposed by Harada et al . (2019), who characterized a new inner envelope protein, DLDG1, with K + /H + exchange activity in an E. coli inverted vesicle assay. Disruption of this protein caused a more sustained NPQ induction and significantly higher 9‐AA accumulation in intact chloroplasts, indicative of an increased thylakoid membrane ∆pH.…”

Olisthodiscus represents a new class of Ochrophyta

“…1993, Harada et al. 2019). Although common in plastid genomes of Chloroplastida, red algae and cryptophytes, the gene was unknown from ochrophytes until its recent discovery in the plastid genomes of synuralean chrysophytes by Kim et al.…”

Lack of plastid‐encoded Ycf10, a homolog of the nuclear‐encoded DLDG1 and the cyanobacterial PxcA, enhances the induction of non‐photochemical quenching in tobacco

“…Fluctuating-Light-Acclimation Protein1 (FLAP1) and its possible interactor, Day Length-dependent Delayed-Greening1 (DLDG1) (Harada et al, 2019;Sato et al, 2017). FLAP1 and DLDG1 are specifically conserved in oxygenic phototrophs including cyanobacteria, algae, and plants.…”