Cooperation of chloroplast ascorbate peroxidases and proton gradient regulation 5 is critical for protecting Arabidopsis plants from photo-oxidative stress.

Kameoka, Takashi; Okayasu, Takaya; Kikuraku, Kana; Ogawa, Takahisa; Sawa, Yoshihiro; Yamamoto, Hiroshi; Ishikawa, Takahiro; Maruta, Takanori

Kameoka, Takashi; Okayasu, Takaya; Kikuraku, Kana; Ogawa, Takahisa; Sawa, Yoshihiro; Yamamoto, Hiroshi; Ishikawa, Takahiro; Maruta, Takanori.

Afiliación

Kameoka T; Graduate School of Natural Science and Technology, Shimane University, 1060 Nishikawatsu, Matsue, Shimane, 690-8504, Japan.
Okayasu T; Department of Life Science and Biotechnology, Faculty of Life and Environmental Science, Shimane University, 1060 Nishikawatsu, Matsue, Shimane, 690-8504, Japan.
Kikuraku K; Department of Life Science and Biotechnology, Faculty of Life and Environmental Science, Shimane University, 1060 Nishikawatsu, Matsue, Shimane, 690-8504, Japan.
Ogawa T; Graduate School of Natural Science and Technology, Shimane University, 1060 Nishikawatsu, Matsue, Shimane, 690-8504, Japan.
Sawa Y; Department of Life Science and Biotechnology, Faculty of Life and Environmental Science, Shimane University, 1060 Nishikawatsu, Matsue, Shimane, 690-8504, Japan.
Yamamoto H; Bioresource and Life Sciences, The United Graduate School of Agricultural Sciences, Tottori University, 4-101 Koyama-Minami, Tottori, Tottori, 680-8553, Japan.
Ishikawa T; Graduate School of Natural Science and Technology, Shimane University, 1060 Nishikawatsu, Matsue, Shimane, 690-8504, Japan.
Maruta T; Department of Life Science and Biotechnology, Faculty of Life and Environmental Science, Shimane University, 1060 Nishikawatsu, Matsue, Shimane, 690-8504, Japan.

Plant J ; 107(3): 876-892, 2021 08.

Article en En | MEDLINE | ID: mdl-34028907

RESUMEN

High-light (HL) stress enhances the production of H2 O2 from the photosynthetic electron transport chain in chloroplasts, potentially causing photo-oxidative damage. Although stromal and thylakoid membrane-bound ascorbate peroxidases (sAPX and tAPX, respectively) are major H2 O2 -scavenging enzymes in chloroplasts, their knockout mutants do not exhibit a visible phenotype under HL stress. Trans-thylakoid proton gradient (∆pH)-dependent mechanisms exist for controlling H2 O2 production from photosynthesis, such as thermal dissipation of light energy and downregulation of electron transfer between photosystems II and I, and these may compensate for the lack of APXs. To test this hypothesis, we focused on a proton gradient regulation 5 (pgr5) mutant, wherein both ∆pH-dependent mechanisms are impaired, and an Arabidopsis sapx tapx double mutant was crossed with the pgr5 single mutant. The sapx tapx pgr5 triple mutant exhibited extreme sensitivity to HL compared with its parental lines. This phenotype was consistent with cellular redox perturbations and enhanced expression of many oxidative stress-responsive genes. These findings demonstrate that the PGR5-dependent mechanisms compensate for chloroplast APXs, and vice versa. An intriguing finding was that the failure of induction of non-photochemical quenching in pgr5 (because of the limitation in ∆pH formation) was partially recovered in sapx tapx pgr5. Further genetic studies suggested that this recovery was dependent on the NADH dehydrogenase-like complex-dependent pathway for cyclic electron flow around photosystem I. Together with data from the sapx tapx npq4 mutant, we discuss the interrelationship between APXs and ∆pH-dependent mechanisms under HL stress.

Asunto(s)

Proteínas de Arabidopsis/metabolismo; Arabidopsis/metabolismo; Ascorbato Peroxidasas/metabolismo; Proteínas de Cloroplastos/metabolismo; Cloroplastos/enzimología; Complejos de Proteína Captadores de Luz/metabolismo; Proteínas del Complejo del Centro de Reacción Fotosintética/metabolismo; Complejo de Proteína del Fotosistema II/metabolismo; Proteínas de las Membranas de los Tilacoides/metabolismo; Antioxidantes; Arabidopsis/efectos de los fármacos; Proteínas de Arabidopsis/genética; Ascorbato Peroxidasas/genética; Proteínas de Cloroplastos/genética; Regulación Enzimológica de la Expresión Génica; Regulación de la Expresión Génica de las Plantas; Concentración de Iones de Hidrógeno; Complejos de Proteína Captadores de Luz/genética; Mutación; Oxidación-Reducción; Fotosíntesis; Proteínas del Complejo del Centro de Reacción Fotosintética/genética; Complejo de Proteína del Fotosistema II/genética; Estrés Fisiológico/efectos de la radiación; Proteínas de las Membranas de los Tilacoides/genética

Palabras clave

Arabidopsis; ascorbate peroxidase; cyclic electron flow; high light; non-photochemical quenching; oxidative stress; proton gradient regulation 5; ∆pH

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Texto completo: 1 Colección: 01-internacional Base de datos: MEDLINE Asunto principal: Cloroplastos / Arabidopsis / Proteínas de Arabidopsis / Proteínas del Complejo del Centro de Reacción Fotosintética / Complejos de Proteína Captadores de Luz / Complejo de Proteína del Fotosistema II / Ascorbato Peroxidasas / Proteínas de Cloroplastos / Proteínas de las Membranas de los Tilacoides Idioma: En Revista: Plant J Asunto de la revista: BIOLOGIA MOLECULAR / BOTANICA Año: 2021 Tipo del documento: Article País de afiliación: Japón Pais de publicación: Reino Unido

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