Kameoka Takashi, Okayasu Takaya, Kikuraku Kana, Ogawa Takahisa, Sawa Yoshihiro, Yamamoto Hiroshi, Ishikawa Takahiro, Maruta Takanori
Graduate School of Natural Science and Technology, Shimane University, 1060 Nishikawatsu, Matsue, Shimane, 690-8504, Japan.
Department of Life Science and Biotechnology, Faculty of Life and Environmental Science, Shimane University, 1060 Nishikawatsu, Matsue, Shimane, 690-8504, Japan.
Plant J. 2021 Aug;107(3):876-892. doi: 10.1111/tpj.15352. Epub 2021 Jun 28.
High-light (HL) stress enhances the production of H O 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 H O -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 H O 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.
高光（HL）胁迫会增强叶绿体中光合电子传递链产生H₂O₂的能力，这可能会导致光氧化损伤。尽管基质型和类囊体膜结合型抗坏血酸过氧化物酶（分别为sAPX和tAPX）是叶绿体中主要的H₂O₂清除酶，但它们的敲除突变体在HL胁迫下并未表现出可见的表型。存在依赖类囊体跨膜质子梯度（∆pH）的机制来控制光合作用产生H₂O₂，例如光能的热耗散以及光系统II和I之间电子传递的下调，这些机制可能弥补了抗坏血酸过氧化物酶（APXs）的缺失。为了验证这一假设，我们重点研究了质子梯度调节5（pgr5）突变体，其中依赖∆pH的两种机制均受损，并且将拟南芥sapx tapx双突变体与pgr5单突变体进行杂交。与亲本系相比，sapx tapx pgr5三突变体对HL表现出极端敏感性。这种表型与细胞氧化还原扰动以及许多氧化应激响应基因的表达增强一致。这些发现表明，依赖PGR5的机制弥补了叶绿体APXs的功能，反之亦然。一个有趣的发现是，pgr5中由于∆pH形成受限而导致的非光化学猝灭诱导失败在sapx tapx pgr5中部分得到恢复。进一步的遗传学研究表明，这种恢复依赖于围绕光系统I的循环电子流的依赖NADH脱氢酶样复合体的途径。结合来自sapx tapx npq4突变体的数据，我们讨论了HL胁迫下APXs与依赖∆pH的机制之间的相互关系。
