title: The Type II NADPH Dehydrogenase Facilitates Cyclic Electron Flow, Energy-Dependent Quenching, and Chlororespiratory Metabolism during Acclimation of Chlamydomonas reinhardtii to Nitrogen Deprivation.
abstract: When photosynthetic organisms are deprived of nitrogen (N), the capacity to grow and assimilate carbon becomes limited, causing a decrease in the productive use of absorbed light energy and likely a rise in the cellular reduction state. Although there is a scarcity of N in many terrestrial and aquatic environments, a mechanistic understanding of how photosynthesis adjusts to low-N conditions and the enzymes/activities integral to these adjustments have not been described. In this work, we use biochemical and biophysical analyses of photoautotrophically grown wild-type and mutant strains of Chlamydomonas reinhardtii to determine the integration of electron transport pathways critical for maintaining active photosynthetic complexes even after exposure of cells to N deprivation for 3 d. Key to acclimation is the type II NADPH dehydrogenase, NDA2, which drives cyclic electron flow (CEF), chlororespiration, and the generation of an H(+) gradient across the thylakoid membranes. N deprivation elicited a doubling of the rate of NDA2-dependent CEF, with little contribution from PGR5/PGRL1-dependent CEF The H(+) gradient generated by CEF is essential to sustain nonphotochemical quenching, while an increase in the level of reduced plastoquinone would promote a state transition; both are necessary to down-regulate photosystem II activity. Moreover, stimulation of NDA2-dependent chlororespiration affords additional relief from the elevated reduction state associated with N deprivation through plastid terminal oxidase-dependent water synthesis. Overall, rerouting electrons through the NDA2 catalytic hub in response to photoautotrophic N deprivation sustains cell viability while promoting the dissipation of excess excitation energy through quenching and chlororespiratory processes.
authors: Department of Plant Biology, Carnegie Institution for Science, Stanford, California 94305 (S.I.S., T.M.W., A.R.G.); andDepartment of Biology, Stanford University, Stanford, California 94305-5020 (T.M.W.) ssaroussi@carnegiescience.edu.
authors: Shai I
authors: 0000-0003-0422-6165
authors: SI
authors: Saroussi
authors: Department of Plant Biology, Carnegie Institution for Science, Stanford, California 94305 (S.I.S., T.M.W., A.R.G.); andDepartment of Biology, Stanford University, Stanford, California 94305-5020 (T.M.W.).
authors: Tyler M
authors: 0000-0001-7061-0611
authors: TM
authors: Wittkopp
authors: Department of Plant Biology, Carnegie Institution for Science, Stanford, California 94305 (S.I.S., T.M.W., A.R.G.); andDepartment of Biology, Stanford University, Stanford, California 94305-5020 (T.M.W.).
authors: Arthur R
authors: AR
authors: Grossman
mesh_terms: D000064:Acclimatization / Q000187:drug effects*; D052818:Autotrophic Processes / Q000187:drug effects / Q000528:radiation effects; D019069:Cell Respiration / Q000187:drug effects; D016825:Chlamydomonas reinhardtii / Q000187:drug effects / Q000502:physiology*; D002736:Chloroplasts / Q000187:drug effects / Q000378:metabolism*; D004579:Electron Transport / Q000187:drug effects / Q000528:radiation effects; D008027:Light; D008954:Models, Biological; D009249:NADP / Q000378:metabolism; D009252:NADPH Dehydrogenase / Q000378:metabolism*; D009584:Nitrogen / Q000494:pharmacology*; D010455:Peptides / Q000378:metabolism; D055668:Photochemical Processes / Q000187:drug effects / Q000528:radiation effects; D010788:Photosynthesis / Q000187:drug effects / Q000528:radiation effects; D045332:Photosystem II Protein Complex / Q000378:metabolism; D052817:Phototrophic Processes / Q000187:drug effects / Q000528:radiation effects; D010858:Pigmentation / Q000187:drug effects / Q000528:radiation effects; D010860:Pigments, Biological / Q000378:metabolism; D010971:Plastoquinone / Q000378:metabolism; D021122:Protein Subunits / Q000378:metabolism; D011522:Protons
chemical_list: D010455:Peptides; D045332:Photosystem II Protein Complex; D010860:Pigments, Biological; D021122:Protein Subunits; D011522:Protons; D009249:NADP; D009252:NADPH Dehydrogenase; D009584:Nitrogen; D010971:Plastoquinone