title: 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 Ca2+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.
authors.affiliation: Institute of Plant Biology and Biotechnology, University of Münster, 48143 Muenster, Germany (B.K., L.M., D.P., J.S., T.B., C.F., M.H.);Centre National Recherche Scientifique, Unité Mixte Recherche 5168, Laboratoire Physiologie Cellulaire et Végétale, F-38054 Grenoble, France (D.P., G.F.);Commissariat à l'Energie Atomique et Energies Alternatives, l'Institut de Recherches en Technologies et Sciences pour le Vivant, F-38054 Grenoble, France (D.P., G.F.);Institut National Recherche Agronomique, Unité Mixte Recherche 1200, F-38054 Grenoble, France (D.P., G.F.);Université Grenoble Alpes, F-38041 Grenoble, France (D.P., G.F.); andDepartment of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, Frederiksberg C 1871, Denmark (M.P.).
authors.forename: Bernadeta
authors.initials: B
authors.lastname: Kukuczka
authors.affiliation: Institute of Plant Biology and Biotechnology, University of Münster, 48143 Muenster, Germany (B.K., L.M., D.P., J.S., T.B., C.F., M.H.);Centre National Recherche Scientifique, Unité Mixte Recherche 5168, Laboratoire Physiologie Cellulaire et Végétale, F-38054 Grenoble, France (D.P., G.F.);Commissariat à l'Energie Atomique et Energies Alternatives, l'Institut de Recherches en Technologies et Sciences pour le Vivant, F-38054 Grenoble, France (D.P., G.F.);Institut National Recherche Agronomique, Unité Mixte Recherche 1200, F-38054 Grenoble, France (D.P., G.F.);Université Grenoble Alpes, F-38041 Grenoble, France (D.P., G.F.); andDepartment of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, Frederiksberg C 1871, Denmark (M.P.).
authors.forename: Leonardo
authors.initials: L
authors.lastname: Magneschi
authors.affiliation: Institute of Plant Biology and Biotechnology, University of Münster, 48143 Muenster, Germany (B.K., L.M., D.P., J.S., T.B., C.F., M.H.);Centre National Recherche Scientifique, Unité Mixte Recherche 5168, Laboratoire Physiologie Cellulaire et Végétale, F-38054 Grenoble, France (D.P., G.F.);Commissariat à l'Energie Atomique et Energies Alternatives, l'Institut de Recherches en Technologies et Sciences pour le Vivant, F-38054 Grenoble, France (D.P., G.F.);Institut National Recherche Agronomique, Unité Mixte Recherche 1200, F-38054 Grenoble, France (D.P., G.F.);Université Grenoble Alpes, F-38041 Grenoble, France (D.P., G.F.); andDepartment of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, Frederiksberg C 1871, Denmark (M.P.).
authors.forename: Dimitris
authors.initials: D
authors.lastname: Petroutsos
authors.affiliation: Institute of Plant Biology and Biotechnology, University of Münster, 48143 Muenster, Germany (B.K., L.M., D.P., J.S., T.B., C.F., M.H.);Centre National Recherche Scientifique, Unité Mixte Recherche 5168, Laboratoire Physiologie Cellulaire et Végétale, F-38054 Grenoble, France (D.P., G.F.);Commissariat à l'Energie Atomique et Energies Alternatives, l'Institut de Recherches en Technologies et Sciences pour le Vivant, F-38054 Grenoble, France (D.P., G.F.);Institut National Recherche Agronomique, Unité Mixte Recherche 1200, F-38054 Grenoble, France (D.P., G.F.);Université Grenoble Alpes, F-38041 Grenoble, France (D.P., G.F.); andDepartment of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, Frederiksberg C 1871, Denmark (M.P.).
authors.forename: Janina
authors.initials: J
authors.lastname: Steinbeck
authors.affiliation: Institute of Plant Biology and Biotechnology, University of Münster, 48143 Muenster, Germany (B.K., L.M., D.P., J.S., T.B., C.F., M.H.);Centre National Recherche Scientifique, Unité Mixte Recherche 5168, Laboratoire Physiologie Cellulaire et Végétale, F-38054 Grenoble, France (D.P., G.F.);Commissariat à l'Energie Atomique et Energies Alternatives, l'Institut de Recherches en Technologies et Sciences pour le Vivant, F-38054 Grenoble, France (D.P., G.F.);Institut National Recherche Agronomique, Unité Mixte Recherche 1200, F-38054 Grenoble, France (D.P., G.F.);Université Grenoble Alpes, F-38041 Grenoble, France (D.P., G.F.); andDepartment of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, Frederiksberg C 1871, Denmark (M.P.).
authors.forename: Till
authors.initials: T
authors.lastname: Bald
authors.affiliation: Institute of Plant Biology and Biotechnology, University of Münster, 48143 Muenster, Germany (B.K., L.M., D.P., J.S., T.B., C.F., M.H.);Centre National Recherche Scientifique, Unité Mixte Recherche 5168, Laboratoire Physiologie Cellulaire et Végétale, F-38054 Grenoble, France (D.P., G.F.);Commissariat à l'Energie Atomique et Energies Alternatives, l'Institut de Recherches en Technologies et Sciences pour le Vivant, F-38054 Grenoble, France (D.P., G.F.);Institut National Recherche Agronomique, Unité Mixte Recherche 1200, F-38054 Grenoble, France (D.P., G.F.);Université Grenoble Alpes, F-38041 Grenoble, France (D.P., G.F.); andDepartment of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, Frederiksberg C 1871, Denmark (M.P.).
authors.forename: Marta
authors.initials: M
authors.lastname: Powikrowska
authors.affiliation: Institute of Plant Biology and Biotechnology, University of Münster, 48143 Muenster, Germany (B.K., L.M., D.P., J.S., T.B., C.F., M.H.);Centre National Recherche Scientifique, Unité Mixte Recherche 5168, Laboratoire Physiologie Cellulaire et Végétale, F-38054 Grenoble, France (D.P., G.F.);Commissariat à l'Energie Atomique et Energies Alternatives, l'Institut de Recherches en Technologies et Sciences pour le Vivant, F-38054 Grenoble, France (D.P., G.F.);Institut National Recherche Agronomique, Unité Mixte Recherche 1200, F-38054 Grenoble, France (D.P., G.F.);Université Grenoble Alpes, F-38041 Grenoble, France (D.P., G.F.); andDepartment of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, Frederiksberg C 1871, Denmark (M.P.).
authors.forename: Christian
authors.initials: C
authors.lastname: Fufezan
authors.affiliation: Institute of Plant Biology and Biotechnology, University of Münster, 48143 Muenster, Germany (B.K., L.M., D.P., J.S., T.B., C.F., M.H.);Centre National Recherche Scientifique, Unité Mixte Recherche 5168, Laboratoire Physiologie Cellulaire et Végétale, F-38054 Grenoble, France (D.P., G.F.);Commissariat à l'Energie Atomique et Energies Alternatives, l'Institut de Recherches en Technologies et Sciences pour le Vivant, F-38054 Grenoble, France (D.P., G.F.);Institut National Recherche Agronomique, Unité Mixte Recherche 1200, F-38054 Grenoble, France (D.P., G.F.);Université Grenoble Alpes, F-38041 Grenoble, France (D.P., G.F.); andDepartment of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, Frederiksberg C 1871, Denmark (M.P.).
authors.forename: Giovanni
authors.initials: G
authors.lastname: Finazzi
authors.affiliation: Institute of Plant Biology and Biotechnology, University of Münster, 48143 Muenster, Germany (B.K., L.M., D.P., J.S., T.B., C.F., M.H.);Centre National Recherche Scientifique, Unité Mixte Recherche 5168, Laboratoire Physiologie Cellulaire et Végétale, F-38054 Grenoble, France (D.P., G.F.);Commissariat à l'Energie Atomique et Energies Alternatives, l'Institut de Recherches en Technologies et Sciences pour le Vivant, F-38054 Grenoble, France (D.P., G.F.);Institut National Recherche Agronomique, Unité Mixte Recherche 1200, F-38054 Grenoble, France (D.P., G.F.);Université Grenoble Alpes, F-38041 Grenoble, France (D.P., G.F.); andDepartment of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, Frederiksberg C 1871, Denmark (M.P.) mhippler@uni-muenster.de.
authors.forename: Michael
authors.initials: M
authors.lastname: Hippler