Proton Gradient Regulation5-Like1-Mediated Cyclic Electron Flow Is Crucial for Acclimation to Anoxia and Complementary to Nonphotochemical Quenching in Stress Adaptation  

Abstract

To investigate the functional importance of Proton Gradient Regulation5-Like1 (PGRL1) for photosynthetic performances in the moss Physcomitrella patens, we generated a pgrl1 knockout mutant. Functional analysis revealed diminished nonphotochemical quenching (NPQ) as well as decreased capacity for cyclic electron flow (CEF) in pgrl1. Under anoxia, where CEF is induced, quantitative proteomics evidenced severe down-regulation of photosystems but up-regulation of the chloroplast NADH dehydrogenase complex, plastocyanin, and Ca 2+ sensors in the mutant, indicating that the absence of PGRL1 triggered a mechanism compensatory for diminished CEF. On the other hand, proteins required for NPQ, such as light-harvesting complex stress-related protein1 (LHCSR1), violaxanthin de-epoxidase, and PSII subunit S, remained stable. To further investigate the interrelation between CEF and NPQ, we generated a pgrl1 npq4 double mutant in the green alga Chlamydomonas reinhardtii lacking both PGRL1 and LHCSR3 expression. Phenotypic comparative analyses of this double mutant, together with the single knockout strains and with the P. patens pgrl1, demonstrated that PGRL1 is crucial for acclimation to high light and anoxia in both organisms. Moreover, the data generated for the C. reinhardtii double mutant clearly showed a complementary role of PGRL1 and LHCSR3 in managing high light stress response. We conclude that both proteins are needed for photoprotection and for survival under low oxygen, underpinning a tight link between CEF and NPQ in oxygenic photosynthesis. Given the complementarity of the energy-dependent component of NPQ (qE) and PGRL1-mediated CEF, we suggest that PGRL1 is a capacitor linked to the evolution of the PSII subunit S-dependent qE in terrestrial plants.The conversion of solar energy into chemical energy and building material by oxygenic photosynthesis, as performed by plants, green algae, and cyanobacteria, supports much of the life on our planet. The production of oxygen and the assimilation of carbon dioxide into organic matter determines, to a large extent, the composition of our atmosphere. Plant photosynthesis is achieved thanks to a series of reactions that occur mainly in the chloroplast, resulting in light-dependent water oxidation, NADP + reduction, and ATP formation (Whatley et al., 1963). Two separate photosystems (PSI and PSII) and an ATP synthase (ATPase) embedded in the thylakoid membrane catalyze these reactions. The ATPase produces ATP at the expense of the proton motive force that is generated by the light reactions (Mitchell, 1961). The cytochrome (cyt) b 6 f complex assures the link between the two photosystems by transferring electrons from the membrane-bound plastoquinone to a soluble carrier, plastocyanin, or cyt c 6 and functions in the pumping of protons. NADPH and ATP that are produced by linear electron flow from PSII to PSI are fueled into the Calvin Benson Bassham cycle (Bassham et al., 1950) to fix CO 2 . In parallel, cyclic electron flow (CEF)

Induction of Photosynthetic Carbon Fixation in Anoxia Relies on Hydrogenase Activity and Proton-Gradient Regulation-Like1-Mediated Cyclic Electron Flow in Chlamydomonas reinhardtii

“…7B). PGRL1-dependent PSI-CEF has been proposed to be crucial for acclimation and survival in anoxic conditions under a constant light regime, both in Physcomitrella patens and C. reinhardtii (Kukuczka et al, 2014). In our experimental conditions, growth of pgrl1 mutant was not impaired (Fig.…”

STATE TRANSITION7-Dependent Phosphorylation Is Modulated by Changing Environmental Conditions, and Its Absence Triggers Remodeling of Photosynthetic Protein Complexes

“…It has been demonstrated that efficient CEF is crucial for successful acclimation to excess light (Munekage et al, 2004;Dang et al, 2014;Johnson et al, 2014;Kukuczka et al, 2014). The most rapid response to excess light, however, relies on a mechanism called nonphotochemical quenching (NPQ).…”

Light-harvesting antenna complexes in the moss Physcomitrella patens: implications for the evolutionary transition from green algae to land plants

“…In P. patens, PGR5/PGRL1-dependent cyclic electron flow appears to operate, based on analyses using the pgrl1 knockout mutant [39 ]. Interestingly, it is also suggested that PGRL1 is required for survival under high light and anoxic conditions in C. reinhardtii and P. patens and thus might have been essential for plant terrestrialization [39 ].…”

“…Interestingly, it is also suggested that PGRL1 is required for survival under high light and anoxic conditions in C. reinhardtii and P. patens and thus might have been essential for plant terrestrialization [39 ]. The NDH complex is absent in green algae and some gymnosperms but present in P. patens.…”