title: Chloroplastic ATP synthase builds up a proton motive force preventing production of reactive oxygen species in photosystem I.
abstract: Over-reduction of the photosynthetic electron transport (PET) chain should be avoided, because the accumulation of reducing electron carriers produces reactive oxygen species (ROS) within photosystem I (PSI) in thylakoid membranes and causes oxidative damage to chloroplasts. To prevent production of ROS in thylakoid membranes the H+gradient (ΔpH) needs to be built up across the thylakoid membranes to suppress the over-reduction state of the PET chain. In this study, we aimed to identify the critical component that stimulates ΔpH formation under illumination in higher plants. To do this, we screened ethyl methane sulfonate (EMS)-treated Arabidopsis thaliana, in which the formation of ΔpH is impaired and the PET chain caused over-reduction under illumination. Subsequently, we isolated an allelic mutant that carries a missense mutation in the γ-subunit of chloroplastic CF0CF1-ATP synthase, named hope2. We found that hope2 suppressed the formation of ΔpH during photosynthesis because of the high H+efflux activity from the lumenal to stromal side of the thylakoid membranes via CF0CF1-ATP synthase. Furthermore, PSI was in a more reduced state in hope2 than in wild-type (WT) plants, and hope2 was more vulnerable to PSI photoinhibition than WT under illumination. These results suggested that chloroplastic CF0CF1-ATP synthase adjusts the redox state of the PET chain, especially for PSI, by modulating H+efflux activity across the thylakoid membranes. Our findings suggest the importance of the buildup of ΔpH depending on CF0CF1-ATP synthase to adjust the redox state of the reaction center chlorophyll P700 in PSI and to suppress the production of ROS in PSI during photosynthesis.
authors.affiliation: Department of Biological and Environmental Science, Faculty of Agriculture, Graduate School of Agricultural Science, Kobe University, 1-1 Rokkodai, Nada, Kobe, 657-8501, Japan.|Core Research for Environmental Science and Technology, Japan Science and Technology Agency, 7 Gobancho, Chiyoda-ku, Tokyo, 102-0076, Japan.
authors.forename: Daisuke
authors.identifier: http://orcid.org/0000-0003-0880-5877
authors.initials: D
authors.lastname: Takagi
authors.affiliation: Faculty of Nutrition, Kobe Gakuin University, Kobe, 651-2180, Japan.
authors.forename: Katsumi
authors.initials: K
authors.lastname: Amako
authors.affiliation: Department of Biological and Environmental Science, Faculty of Agriculture, Graduate School of Agricultural Science, Kobe University, 1-1 Rokkodai, Nada, Kobe, 657-8501, Japan.
authors.forename: Masaki
authors.initials: M
authors.lastname: Hashiguchi
authors.affiliation: Department of Biology, Graduate School of Science, Kobe University, 1-1 Rokkodai, Nada-ku, Kobe, 657-8501, Japan.
authors.forename: Hidehiro
authors.initials: H
authors.lastname: Fukaki
authors.affiliation: Department of Biology, Graduate School of Science, Kobe University, 1-1 Rokkodai, Nada-ku, Kobe, 657-8501, Japan.
authors.forename: Kimitsune
authors.initials: K
authors.lastname: Ishizaki
authors.affiliation: Department of Biology, Graduate School of Science, Kobe University, 1-1 Rokkodai, Nada-ku, Kobe, 657-8501, Japan.
authors.forename: Tatsuaki
authors.initials: T
authors.lastname: Goh
authors.affiliation: Graduate School of Biological Sciences, Nara Institute of Science and Technology (NAIST), Ikoma, 630-0192, Japan.
authors.forename: Yoichiro
authors.initials: Y
authors.lastname: Fukao
authors.affiliation: Graduate School of Biological Sciences, Nara Institute of Science and Technology (NAIST), Ikoma, 630-0192, Japan.
authors.forename: Ryosuke
authors.initials: R
authors.lastname: Sano
authors.affiliation: Graduate School of Biological Sciences, Nara Institute of Science and Technology (NAIST), Ikoma, 630-0192, Japan.|Graduate School of Life Sciences, Tohoku University, Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai, 980-8578, Japan.
authors.forename: Tetsuya
authors.initials: T
authors.lastname: Kurata
authors.affiliation: Graduate School of Biological Sciences, Nara Institute of Science and Technology (NAIST), Ikoma, 630-0192, Japan.
authors.forename: Taku
authors.initials: T
authors.lastname: Demura
authors.affiliation: Graduate School of Science and Technology, Kumamoto University, Kurokami, Tyuou-ku, Kumamoto, 860-8555, Japan.
authors.forename: Shinichiro
authors.initials: S
authors.lastname: Sawa
authors.affiliation: Department of Biological and Environmental Science, Faculty of Agriculture, Graduate School of Agricultural Science, Kobe University, 1-1 Rokkodai, Nada, Kobe, 657-8501, Japan.|Core Research for Environmental Science and Technology, Japan Science and Technology Agency, 7 Gobancho, Chiyoda-ku, Tokyo, 102-0076, Japan.
authors.forename: Chikahiro
authors.initials: C
authors.lastname: Miyake
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D025222:Chloroplast Proton-Translocating ATPases / Q000235:genetics / Q000378:metabolism*; D004579:Electron Transport; D008027:Light; D009154:Mutation; D010788:Photosynthesis; D045331:Photosystem I Protein Complex / Q000378:metabolism*; D018892:Proton-Motive Force; D017382:Reactive Oxygen Species / Q000378:metabolism*; D020524:Thylakoids / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D045331:Photosystem I Protein Complex; D017382:Reactive Oxygen Species; C000625626:ATPC1 protein, Arabidopsis; D025222:Chloroplast Proton-Translocating ATPases
keywords: CF0CF1-ATP synthase; photoinhibition; photosystem I; reactive oxygen species; ΔpH