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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Main Authors: Zhenxiang Jiang, Chihiro K. A. Watanabe, Atsuko Miyagi, Maki Kawai-Yamada, Ichiro Terashima, Ko Noguchi
Format: Article
Language:English
Published: MDPI AG 2019-06-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/20/12/3067
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spelling 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 &#947;-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 &#947;-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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