Modulating the activities of chloroplasts and mitochondria promotes adenosine triphosphate production and plant growth

Efficient photosynthesis requires a balance of ATP and NADPH production/consumption in chloroplasts, and the exportation of reducing equivalents from chloroplasts is important for balancing stromal ATP/NADPH ratio. Here, we showed that the overexpression of purple acid phosphatase 2 on the outer mem...

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Main Authors: Chia P. Voon, Yee-Song Law, Xiaoqian Guan, Shey-Li Lim, Zhou Xu, Wing-Tung Chu, Renshan Zhang, Feng Sun, Mathias Labs, Dario Leister, Mathias Pribil, Marie Hronková, Jiří Kubásek, Yong Cui, Liwen Jiang, Michito Tsuyama, Per Gardeström, Mikko Tikkanen, Boon L. Lim
Format: Article
Language:English
Published: Cambridge University Press 2021-01-01
Series:Quantitative Plant Biology
Subjects:
Online Access:https://www.cambridge.org/core/product/identifier/S2632882821000072/type/journal_article
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author Chia P. Voon
Yee-Song Law
Xiaoqian Guan
Shey-Li Lim
Zhou Xu
Wing-Tung Chu
Renshan Zhang
Feng Sun
Mathias Labs
Dario Leister
Mathias Pribil
Marie Hronková
Jiří Kubásek
Yong Cui
Liwen Jiang
Michito Tsuyama
Per Gardeström
Mikko Tikkanen
Boon L. Lim
author_facet Chia P. Voon
Yee-Song Law
Xiaoqian Guan
Shey-Li Lim
Zhou Xu
Wing-Tung Chu
Renshan Zhang
Feng Sun
Mathias Labs
Dario Leister
Mathias Pribil
Marie Hronková
Jiří Kubásek
Yong Cui
Liwen Jiang
Michito Tsuyama
Per Gardeström
Mikko Tikkanen
Boon L. Lim
author_sort Chia P. Voon
collection DOAJ
description Efficient photosynthesis requires a balance of ATP and NADPH production/consumption in chloroplasts, and the exportation of reducing equivalents from chloroplasts is important for balancing stromal ATP/NADPH ratio. Here, we showed that the overexpression of purple acid phosphatase 2 on the outer membranes of chloroplasts and mitochondria can streamline the production and consumption of reducing equivalents in these two organelles, respectively. A higher capacity of consumption of reducing equivalents in mitochondria can indirectly help chloroplasts to balance the ATP/NADPH ratio in stroma and recycle NADP+, the electron acceptors of the linear electron flow (LEF). A higher rate of ATP and NADPH production from the LEF, a higher capacity of carbon fixation by the Calvin–Benson–Bassham (CBB) cycle and a greater consumption of NADH in mitochondria enhance photosynthesis in the chloroplasts, ATP production in the mitochondria and sucrose synthesis in the cytosol and eventually boost plant growth and seed yields in the overexpression lines.
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spelling doaj.art-8a4e34b83f5b42f582b488be11cdbe182023-03-09T12:43:33ZengCambridge University PressQuantitative Plant Biology2632-88282021-01-01210.1017/qpb.2021.7Modulating the activities of chloroplasts and mitochondria promotes adenosine triphosphate production and plant growthChia P. Voon0Yee-Song Law1Xiaoqian Guan2Shey-Li Lim3Zhou Xu4Wing-Tung Chu5Renshan Zhang6Feng Sun7Mathias Labs8Dario Leister9Mathias Pribil10Marie Hronková11Jiří Kubásek12Yong Cui13Liwen Jiang14Michito Tsuyama15Per Gardeström16Mikko Tikkanen17Boon L. Lim18https://orcid.org/0000-0002-2720-2353School of Biological Sciences, The University of Hong Kong, Pokfulam, ChinaSchool of Biological Sciences, The University of Hong Kong, Pokfulam, ChinaSchool of Biological Sciences, The University of Hong Kong, Pokfulam, ChinaSchool of Biological Sciences, The University of Hong Kong, Pokfulam, ChinaSchool of Biological Sciences, The University of Hong Kong, Pokfulam, ChinaSchool of Biological Sciences, The University of Hong Kong, Pokfulam, ChinaSchool of Biological Sciences, The University of Hong Kong, Pokfulam, ChinaSchool of Biological Sciences, The University of Hong Kong, Pokfulam, ChinaPlant Molecular Biology, Department of Biology, Ludwig-Maximilians-University Munich (LMU), Munich, GermanyPlant Molecular Biology, Department of Biology, Ludwig-Maximilians-University Munich (LMU), Munich, GermanyCopenhagen Plant Science Centre, Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, DenmarkFaculty of Science, University of South Bohemia, Ceske Budejovice, Czech RepublicFaculty of Science, University of South Bohemia, Ceske Budejovice, Czech RepublicSchool of Life Sciences, Centre for Cell and Developmental Biology, The Chinese University of Hong Kong, Shatin, China State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin, ChinaSchool of Life Sciences, Centre for Cell and Developmental Biology, The Chinese University of Hong Kong, Shatin, China State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin, ChinaDepartment of Agriculture, Kyushu University, Fukuoka, JapanUmeå Plant Science Centre, Department of Plant Physiology, Umeå University, Umeå, SwedenMolecular Plant Biology, Department of Life Technologies, University of Turku, Turku, FinlandSchool of Biological Sciences, The University of Hong Kong, Pokfulam, China School of Life Sciences, Centre for Cell and Developmental Biology, The Chinese University of Hong Kong, Shatin, China State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin, ChinaEfficient photosynthesis requires a balance of ATP and NADPH production/consumption in chloroplasts, and the exportation of reducing equivalents from chloroplasts is important for balancing stromal ATP/NADPH ratio. Here, we showed that the overexpression of purple acid phosphatase 2 on the outer membranes of chloroplasts and mitochondria can streamline the production and consumption of reducing equivalents in these two organelles, respectively. A higher capacity of consumption of reducing equivalents in mitochondria can indirectly help chloroplasts to balance the ATP/NADPH ratio in stroma and recycle NADP+, the electron acceptors of the linear electron flow (LEF). A higher rate of ATP and NADPH production from the LEF, a higher capacity of carbon fixation by the Calvin–Benson–Bassham (CBB) cycle and a greater consumption of NADH in mitochondria enhance photosynthesis in the chloroplasts, ATP production in the mitochondria and sucrose synthesis in the cytosol and eventually boost plant growth and seed yields in the overexpression lines.https://www.cambridge.org/core/product/identifier/S2632882821000072/type/journal_articleATPAtPAP2chloroplastsmitochondriaNADPHphotosynthesis
spellingShingle Chia P. Voon
Yee-Song Law
Xiaoqian Guan
Shey-Li Lim
Zhou Xu
Wing-Tung Chu
Renshan Zhang
Feng Sun
Mathias Labs
Dario Leister
Mathias Pribil
Marie Hronková
Jiří Kubásek
Yong Cui
Liwen Jiang
Michito Tsuyama
Per Gardeström
Mikko Tikkanen
Boon L. Lim
Modulating the activities of chloroplasts and mitochondria promotes adenosine triphosphate production and plant growth
Quantitative Plant Biology
ATP
AtPAP2
chloroplasts
mitochondria
NADPH
photosynthesis
title Modulating the activities of chloroplasts and mitochondria promotes adenosine triphosphate production and plant growth
title_full Modulating the activities of chloroplasts and mitochondria promotes adenosine triphosphate production and plant growth
title_fullStr Modulating the activities of chloroplasts and mitochondria promotes adenosine triphosphate production and plant growth
title_full_unstemmed Modulating the activities of chloroplasts and mitochondria promotes adenosine triphosphate production and plant growth
title_short Modulating the activities of chloroplasts and mitochondria promotes adenosine triphosphate production and plant growth
title_sort modulating the activities of chloroplasts and mitochondria promotes adenosine triphosphate production and plant growth
topic ATP
AtPAP2
chloroplasts
mitochondria
NADPH
photosynthesis
url https://www.cambridge.org/core/product/identifier/S2632882821000072/type/journal_article
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