Mitochondrial AOX Supports Redox Balance of Photosynthetic Electron Transport, Primary Metabolite Balance, and Growth in <i>Arabidopsis thaliana</i> under High Light
When leaves receive excess light energy, excess reductants accumulate in chloroplasts. It is suggested that some of the reductants are oxidized by the mitochondrial respiratory chain. Alternative oxidase (AOX), a non-energy conserving terminal oxidase, was upregulated in the photosynthetic mutant of...
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doaj-72c3243626664612932c26435788642e2020-11-25T01:40:37ZengMDPI AGInternational Journal of Molecular Sciences1422-00672019-06-012012306710.3390/ijms20123067ijms20123067Mitochondrial AOX Supports Redox Balance of Photosynthetic Electron Transport, Primary Metabolite Balance, and Growth in <i>Arabidopsis thaliana</i> under High LightZhenxiang Jiang0Chihiro K. A. Watanabe1Atsuko Miyagi2Maki Kawai-Yamada3Ichiro Terashima4Ko Noguchi5Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, JapanDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, JapanGraduate School of Science and Engineering, Saitama University, 225 Shimo-Okubo, Sakura-ku, Saitama-city, Saitama 338-8570, JapanGraduate School of Science and Engineering, Saitama University, 225 Shimo-Okubo, Sakura-ku, Saitama-city, Saitama 338-8570, JapanDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, JapanSchool of Life Sciences, Tokyo University of Pharmacy and Life Sciences, 1432-1 Horinouchi, Hachioji, Tokyo 192-0392, JapanWhen leaves receive excess light energy, excess reductants accumulate in chloroplasts. It is suggested that some of the reductants are oxidized by the mitochondrial respiratory chain. Alternative oxidase (AOX), a non-energy conserving terminal oxidase, was upregulated in the photosynthetic mutant of <i>Arabidopsis thaliana</i>, <i>pgr5</i>, which accumulated reductants in chloroplast stroma. AOX is suggested to have an important role in dissipating reductants under high light (HL) conditions, but its physiological importance and underlying mechanisms are not yet known. Here, we compared wild-type (WT), <i>pgr5</i>, and a double mutant of AOX1a-knockout plant (<i>aox1a</i>) and <i>pgr5</i> (<i>aox1a/pgr5</i>) grown under high- and low-light conditions, and conducted physiological analyses. The net assimilation rate (<i>NAR</i>) was lower in <i>aox1a/pgr5</i> than that in the other genotypes at the early growth stage, while the leaf area ratio was higher in <i>aox1a/pgr5</i>. We assessed detailed mechanisms in relation to <i>NAR</i>. In <i>aox1a/pgr5</i>, photosystem II parameters decreased under HL, whereas respiratory O<sub>2</sub> uptake rates increased. Some intermediates in the tricarboxylic acid (TCA) cycle and Calvin cycle decreased in <i>aox1a/pgr5</i>, whereas γ-aminobutyric acid (GABA) and N-rich amino acids increased in <i>aox1a/pgr5</i>. Under HL, AOX may have an important role in dissipating excess reductants to prevent the reduction of photosynthetic electron transport and imbalance in primary metabolite levels.https://www.mdpi.com/1422-0067/20/12/3067alternative oxidasemetabolic interactionmitochondrial respiratory chainphotosynthesisredox balance |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Zhenxiang Jiang Chihiro K. A. Watanabe Atsuko Miyagi Maki Kawai-Yamada Ichiro Terashima Ko Noguchi |
spellingShingle |
Zhenxiang Jiang Chihiro K. A. Watanabe Atsuko Miyagi Maki Kawai-Yamada Ichiro Terashima Ko Noguchi Mitochondrial AOX Supports Redox Balance of Photosynthetic Electron Transport, Primary Metabolite Balance, and Growth in <i>Arabidopsis thaliana</i> under High Light International Journal of Molecular Sciences alternative oxidase metabolic interaction mitochondrial respiratory chain photosynthesis redox balance |
author_facet |
Zhenxiang Jiang Chihiro K. A. Watanabe Atsuko Miyagi Maki Kawai-Yamada Ichiro Terashima Ko Noguchi |
author_sort |
Zhenxiang Jiang |
title |
Mitochondrial AOX Supports Redox Balance of Photosynthetic Electron Transport, Primary Metabolite Balance, and Growth in <i>Arabidopsis thaliana</i> under High Light |
title_short |
Mitochondrial AOX Supports Redox Balance of Photosynthetic Electron Transport, Primary Metabolite Balance, and Growth in <i>Arabidopsis thaliana</i> under High Light |
title_full |
Mitochondrial AOX Supports Redox Balance of Photosynthetic Electron Transport, Primary Metabolite Balance, and Growth in <i>Arabidopsis thaliana</i> under High Light |
title_fullStr |
Mitochondrial AOX Supports Redox Balance of Photosynthetic Electron Transport, Primary Metabolite Balance, and Growth in <i>Arabidopsis thaliana</i> under High Light |
title_full_unstemmed |
Mitochondrial AOX Supports Redox Balance of Photosynthetic Electron Transport, Primary Metabolite Balance, and Growth in <i>Arabidopsis thaliana</i> under High Light |
title_sort |
mitochondrial aox supports redox balance of photosynthetic electron transport, primary metabolite balance, and growth in <i>arabidopsis thaliana</i> under high light |
publisher |
MDPI AG |
series |
International Journal of Molecular Sciences |
issn |
1422-0067 |
publishDate |
2019-06-01 |
description |
When leaves receive excess light energy, excess reductants accumulate in chloroplasts. It is suggested that some of the reductants are oxidized by the mitochondrial respiratory chain. Alternative oxidase (AOX), a non-energy conserving terminal oxidase, was upregulated in the photosynthetic mutant of <i>Arabidopsis thaliana</i>, <i>pgr5</i>, which accumulated reductants in chloroplast stroma. AOX is suggested to have an important role in dissipating reductants under high light (HL) conditions, but its physiological importance and underlying mechanisms are not yet known. Here, we compared wild-type (WT), <i>pgr5</i>, and a double mutant of AOX1a-knockout plant (<i>aox1a</i>) and <i>pgr5</i> (<i>aox1a/pgr5</i>) grown under high- and low-light conditions, and conducted physiological analyses. The net assimilation rate (<i>NAR</i>) was lower in <i>aox1a/pgr5</i> than that in the other genotypes at the early growth stage, while the leaf area ratio was higher in <i>aox1a/pgr5</i>. We assessed detailed mechanisms in relation to <i>NAR</i>. In <i>aox1a/pgr5</i>, photosystem II parameters decreased under HL, whereas respiratory O<sub>2</sub> uptake rates increased. Some intermediates in the tricarboxylic acid (TCA) cycle and Calvin cycle decreased in <i>aox1a/pgr5</i>, whereas γ-aminobutyric acid (GABA) and N-rich amino acids increased in <i>aox1a/pgr5</i>. Under HL, AOX may have an important role in dissipating excess reductants to prevent the reduction of photosynthetic electron transport and imbalance in primary metabolite levels. |
topic |
alternative oxidase metabolic interaction mitochondrial respiratory chain photosynthesis redox balance |
url |
https://www.mdpi.com/1422-0067/20/12/3067 |
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