Photoinhibition of Photosystem I Provides Oxidative Protection During Imbalanced Photosynthetic Electron Transport in Arabidopsis thaliana

Photosynthesis involves the conversion of sunlight energy into stored chemical energy, which is achieved through electron transport along a series of redox reactions. Excess photosynthetic electron transport might be dangerous due to the risk of molecular oxygen reduction, generating reactive oxygen...

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Main Authors: Yugo Lima-Melo, Vicente T. C. B. Alencar, Ana K. M. Lobo, Rachel H. V. Sousa, Mikko Tikkanen, Eva-Mari Aro, Joaquim A. G. Silveira, Peter J. Gollan
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-07-01
Series:Frontiers in Plant Science
Subjects:
ROS
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2019.00916/full
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spelling doaj-262c9c62670141a3aae58a1e01bedd432020-11-24T21:34:58ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-07-011010.3389/fpls.2019.00916459034Photoinhibition of Photosystem I Provides Oxidative Protection During Imbalanced Photosynthetic Electron Transport in Arabidopsis thalianaYugo Lima-Melo0Yugo Lima-Melo1Vicente T. C. B. Alencar2Ana K. M. Lobo3Rachel H. V. Sousa4Mikko Tikkanen5Eva-Mari Aro6Joaquim A. G. Silveira7Peter J. Gollan8Department of Biochemistry and Molecular Biology, Federal University of Ceará, Fortaleza, BrazilMolecular Plant Biology, Department of Biochemistry, University of Turku, Turku, FinlandDepartment of Biochemistry and Molecular Biology, Federal University of Ceará, Fortaleza, BrazilDepartment of Biochemistry and Molecular Biology, Federal University of Ceará, Fortaleza, BrazilDepartment of Biochemistry and Molecular Biology, Federal University of Ceará, Fortaleza, BrazilMolecular Plant Biology, Department of Biochemistry, University of Turku, Turku, FinlandMolecular Plant Biology, Department of Biochemistry, University of Turku, Turku, FinlandDepartment of Biochemistry and Molecular Biology, Federal University of Ceará, Fortaleza, BrazilMolecular Plant Biology, Department of Biochemistry, University of Turku, Turku, FinlandPhotosynthesis involves the conversion of sunlight energy into stored chemical energy, which is achieved through electron transport along a series of redox reactions. Excess photosynthetic electron transport might be dangerous due to the risk of molecular oxygen reduction, generating reactive oxygen species (ROS) over-accumulation. Avoiding excess ROS production requires the rate of electron transport to be coordinated with the capacity of electron acceptors in the chloroplast stroma. Imbalance between the donor and acceptor sides of photosystem I (PSI) can lead to inactivation, which is called PSI photoinhibition. We used a light-inducible PSI photoinhibition system in Arabidopsis thaliana to resolve the time dynamics of inhibition and to investigate its impact on ROS production and turnover. The oxidation state of the PSI reaction center and rates of CO2 fixation both indicated strong and rapid PSI photoinhibition upon donor side/acceptor side imbalance, while the rate of inhibition eased during prolonged imbalance. PSI photoinhibition was not associated with any major changes in ROS accumulation or antioxidant activity; however, a lower level of lipid oxidation correlated with lower abundance of chloroplast lipoxygenase in PSI-inhibited leaves. The results of this study suggest that rapid activation of PSI photoinhibition under severe photosynthetic imbalance protects the chloroplast from over-reduction and excess ROS formation.https://www.frontiersin.org/article/10.3389/fpls.2019.00916/fullphotosystem IphotosynthesisROSCO2 fixationphotoinhibitionP700
collection DOAJ
language English
format Article
sources DOAJ
author Yugo Lima-Melo
Yugo Lima-Melo
Vicente T. C. B. Alencar
Ana K. M. Lobo
Rachel H. V. Sousa
Mikko Tikkanen
Eva-Mari Aro
Joaquim A. G. Silveira
Peter J. Gollan
spellingShingle Yugo Lima-Melo
Yugo Lima-Melo
Vicente T. C. B. Alencar
Ana K. M. Lobo
Rachel H. V. Sousa
Mikko Tikkanen
Eva-Mari Aro
Joaquim A. G. Silveira
Peter J. Gollan
Photoinhibition of Photosystem I Provides Oxidative Protection During Imbalanced Photosynthetic Electron Transport in Arabidopsis thaliana
Frontiers in Plant Science
photosystem I
photosynthesis
ROS
CO2 fixation
photoinhibition
P700
author_facet Yugo Lima-Melo
Yugo Lima-Melo
Vicente T. C. B. Alencar
Ana K. M. Lobo
Rachel H. V. Sousa
Mikko Tikkanen
Eva-Mari Aro
Joaquim A. G. Silveira
Peter J. Gollan
author_sort Yugo Lima-Melo
title Photoinhibition of Photosystem I Provides Oxidative Protection During Imbalanced Photosynthetic Electron Transport in Arabidopsis thaliana
title_short Photoinhibition of Photosystem I Provides Oxidative Protection During Imbalanced Photosynthetic Electron Transport in Arabidopsis thaliana
title_full Photoinhibition of Photosystem I Provides Oxidative Protection During Imbalanced Photosynthetic Electron Transport in Arabidopsis thaliana
title_fullStr Photoinhibition of Photosystem I Provides Oxidative Protection During Imbalanced Photosynthetic Electron Transport in Arabidopsis thaliana
title_full_unstemmed Photoinhibition of Photosystem I Provides Oxidative Protection During Imbalanced Photosynthetic Electron Transport in Arabidopsis thaliana
title_sort photoinhibition of photosystem i provides oxidative protection during imbalanced photosynthetic electron transport in arabidopsis thaliana
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2019-07-01
description Photosynthesis involves the conversion of sunlight energy into stored chemical energy, which is achieved through electron transport along a series of redox reactions. Excess photosynthetic electron transport might be dangerous due to the risk of molecular oxygen reduction, generating reactive oxygen species (ROS) over-accumulation. Avoiding excess ROS production requires the rate of electron transport to be coordinated with the capacity of electron acceptors in the chloroplast stroma. Imbalance between the donor and acceptor sides of photosystem I (PSI) can lead to inactivation, which is called PSI photoinhibition. We used a light-inducible PSI photoinhibition system in Arabidopsis thaliana to resolve the time dynamics of inhibition and to investigate its impact on ROS production and turnover. The oxidation state of the PSI reaction center and rates of CO2 fixation both indicated strong and rapid PSI photoinhibition upon donor side/acceptor side imbalance, while the rate of inhibition eased during prolonged imbalance. PSI photoinhibition was not associated with any major changes in ROS accumulation or antioxidant activity; however, a lower level of lipid oxidation correlated with lower abundance of chloroplast lipoxygenase in PSI-inhibited leaves. The results of this study suggest that rapid activation of PSI photoinhibition under severe photosynthetic imbalance protects the chloroplast from over-reduction and excess ROS formation.
topic photosystem I
photosynthesis
ROS
CO2 fixation
photoinhibition
P700
url https://www.frontiersin.org/article/10.3389/fpls.2019.00916/full
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