title: Photosynthesis Activates Plasma Membrane H+-ATPase via Sugar Accumulation.
abstract: Plant plasma membrane H(+)-ATPase acts as a primary transporter via proton pumping and regulates diverse physiological responses by controlling secondary solute transport, pH homeostasis, and membrane potential. Phosphorylation of the penultimate threonine and the subsequent binding of 14-3-3 proteins in the carboxyl terminus of the enzyme are required for H(+)-ATPase activation. We showed previously that photosynthesis induces phosphorylation of the penultimate threonine in the nonvascular bryophyte Marchantia polymorpha However, (1) whether this response is conserved in vascular plants and (2) the process by which photosynthesis regulates H(+)-ATPase phosphorylation at the plasma membrane remain unresolved issues. Here, we report that photosynthesis induced the phosphorylation and activation of H(+)-ATPase in Arabidopsis (Arabidopsis thaliana) leaves via sugar accumulation. Light reversibly phosphorylated leaf H(+)-ATPase, and this process was inhibited by pharmacological and genetic suppression of photosynthesis. Immunohistochemical and biochemical analyses indicated that light-induced phosphorylation of H(+)-ATPase occurred autonomously in mesophyll cells. We also show that the phosphorylation status of H(+)-ATPase and photosynthetic sugar accumulation in leaves were positively correlated and that sugar treatment promoted phosphorylation. Furthermore, light-induced phosphorylation of H(+)-ATPase was strongly suppressed in a double mutant defective in ADP-glucose pyrophosphorylase and triose phosphate/phosphate translocator (adg1-1 tpt-2); these mutations strongly inhibited endogenous sugar accumulation. Overall, we show that photosynthesis activated H(+)-ATPase via sugar production in the mesophyll cells of vascular plants. Our work provides new insight into signaling from chloroplasts to the plasma membrane ion transport mechanism.
authors.affiliation: Division of Biological Science, Graduate School of Science (M.O., S.I., T.K.), and Institute of Transformative Bio-Molecules (K.K., T.K.), Nagoya University, Chikusa, Nagoya 464-8602, Japan.
authors.forename: Masaki
authors.initials: M
authors.lastname: Okumura
authors.affiliation: Division of Biological Science, Graduate School of Science (M.O., S.I., T.K.), and Institute of Transformative Bio-Molecules (K.K., T.K.), Nagoya University, Chikusa, Nagoya 464-8602, Japan.
authors.forename: Shin-Ichiro
authors.initials: S
authors.lastname: Inoue
authors.affiliation: Division of Biological Science, Graduate School of Science (M.O., S.I., T.K.), and Institute of Transformative Bio-Molecules (K.K., T.K.), Nagoya University, Chikusa, Nagoya 464-8602, Japan.
authors.forename: Keiko
authors.initials: K
authors.lastname: Kuwata
authors.affiliation: Division of Biological Science, Graduate School of Science (M.O., S.I., T.K.), and Institute of Transformative Bio-Molecules (K.K., T.K.), Nagoya University, Chikusa, Nagoya 464-8602, Japan kinoshita@bio.nagoya-u.ac.jp.
authors.forename: Toshinori
authors.identifier: 0000-0001-7621-1259
authors.initials: T
authors.lastname: Kinoshita
mesh_terms: D049069:ATP-Dependent Proteases / Q000235:genetics / Q000378:metabolism; D017360:Arabidopsis / Q000187:drug effects / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D002462:Cell Membrane / Q000378:metabolism*; D004237:Diuron / Q000494:pharmacology; D008027:Light; D008565:Membrane Proteins / Q000235:genetics / Q000378:metabolism; D026901:Membrane Transport Proteins / Q000235:genetics / Q000378:metabolism; D058503:Mesophyll Cells / Q000378:metabolism; D009154:Mutation; D010766:Phosphorylation; D010788:Photosynthesis / Q000502:physiology*; D018515:Plant Leaves / Q000378:metabolism; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D030821:Plants, Genetically Modified; D006180:Proton-Translocating ATPases / Q000235:genetics / Q000378:metabolism*; D000073893:Sugars / Q000378:metabolism*
chemical_list: D049069:ATP-Dependent Proteases; D029681:Arabidopsis Proteins; D004237:Diuron; D008565:Membrane Proteins; D026901:Membrane Transport Proteins; D010940:Plant Proteins; D006180:Proton-Translocating ATPases; D000073893:Sugars; C078729:sucrose transport protein, plant; C402651:AT2G30950 protein, Arabidopsis