Mutation of the Atypical Kinase ABC1K3 Partially Rescues the PROTON GRADIENT REGULATION 6 Phenotype in Arabidopsis thaliana

Photosynthesis is an essential pathway providing the chemical energy and reducing equivalents that sustain higher plant metabolism. It relies on sunlight, which is an inconstant source of energy that fluctuates in both intensity and spectrum. The fine and rapid tuning of the photosynthetic apparatus...

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Main Authors: Thibaut Pralon, Joy Collombat, Rosa Pipitone, Brigitte Ksas, Venkatasalam Shanmugabalaji, Michel Havaux, Giovanni Finazzi, Paolo Longoni, Felix Kessler
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-03-01
Series:Frontiers in Plant Science
Subjects:
NPQ
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2020.00337/full
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spelling doaj-d9a6e15321374725aefb1ef9f7e8ec532020-11-25T02:38:29ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-03-011110.3389/fpls.2020.00337515340Mutation of the Atypical Kinase ABC1K3 Partially Rescues the PROTON GRADIENT REGULATION 6 Phenotype in Arabidopsis thalianaThibaut Pralon0Joy Collombat1Rosa Pipitone2Brigitte Ksas3Venkatasalam Shanmugabalaji4Michel Havaux5Giovanni Finazzi6Paolo Longoni7Felix Kessler8Laboratory of Plant Physiology, Institute Biology, University of Neuchâtel, Neuchâtel, SwitzerlandLaboratory of Plant Physiology, Institute Biology, University of Neuchâtel, Neuchâtel, SwitzerlandLaboratory of Plant Physiology, Institute Biology, University of Neuchâtel, Neuchâtel, SwitzerlandAix Marseille University, Centre National de la Recherche Scientifique (CNRS), Commissariat à l’Énergie Atomique et aux Énergies Alternatives (CEA), UMR 7265, Biosciences et Biotechnologies Institute of Aix-Marseille, Saint-Paul-lez-Durance, FranceLaboratory of Plant Physiology, Institute Biology, University of Neuchâtel, Neuchâtel, SwitzerlandAix Marseille University, Centre National de la Recherche Scientifique (CNRS), Commissariat à l’Énergie Atomique et aux Énergies Alternatives (CEA), UMR 7265, Biosciences et Biotechnologies Institute of Aix-Marseille, Saint-Paul-lez-Durance, FranceUniversité Grenoble Alpes, Centre National de la Recherche Scientifique (CNRS), Commissariat à l’Énergie Atomique et aux Énergies Alternatives (CEA), Institut National de la Recherche Agromique (INRA), Interdisciplinary Research Institute of Grenoble - Cell and Plant Physiology Laboratory (IRIG-LPCV), Grenoble, FranceLaboratory of Plant Physiology, Institute Biology, University of Neuchâtel, Neuchâtel, SwitzerlandLaboratory of Plant Physiology, Institute Biology, University of Neuchâtel, Neuchâtel, SwitzerlandPhotosynthesis is an essential pathway providing the chemical energy and reducing equivalents that sustain higher plant metabolism. It relies on sunlight, which is an inconstant source of energy that fluctuates in both intensity and spectrum. The fine and rapid tuning of the photosynthetic apparatus is essential to cope with changing light conditions and increase plant fitness. Recently PROTON GRADIENT REGULATION 6 (PGR6-ABC1K1), an atypical plastoglobule-associated kinase, was shown to regulate a new mechanism of light response by controlling the homeostasis of photoactive plastoquinone (PQ). PQ is a crucial electron carrier existing as a free neutral lipid in the photosynthetic thylakoid membrane. Perturbed homeostasis of PQ impairs photosynthesis and plant acclimation to high light. Here we show that a homologous kinase, ABC1K3, which like PGR6-ABC1K1 is associated with plastoglobules, also contributes to the homeostasis of the photoactive PQ pool. Contrary to PGR6-ABC1K1, ABC1K3 disfavors PQ availability for photosynthetic electron transport. In fact, in the abc1k1/abc1k3 double mutant the pgr6(abc1k1) the photosynthetic defect seen in the abc1k1 mutant is mitigated. However, the PQ concentration in the photoactive pool of the double mutant is comparable to that of abc1k1 mutant. An increase of the PQ mobility, inferred from the kinetics of its oxidation in dark, contributes to the mitigation of the pgr6(abc1k1) photosynthetic defect. Our results also demonstrate that ABC1K3 contributes to the regulation of other mechanisms involved in the adaptation of the photosynthetic apparatus to changes in light quality and intensity such as the induction of thermal dissipation and state transitions. Overall, we suggests that, besides the absolute concentration of PQ, its mobility and exchange between storage and active pools are critical for light acclimation in plants.https://www.frontiersin.org/article/10.3389/fpls.2020.00337/fullphotosynthetic electron transportplastoquinone poolplastoglobulehigh light acclimationNPQ
collection DOAJ
language English
format Article
sources DOAJ
author Thibaut Pralon
Joy Collombat
Rosa Pipitone
Brigitte Ksas
Venkatasalam Shanmugabalaji
Michel Havaux
Giovanni Finazzi
Paolo Longoni
Felix Kessler
spellingShingle Thibaut Pralon
Joy Collombat
Rosa Pipitone
Brigitte Ksas
Venkatasalam Shanmugabalaji
Michel Havaux
Giovanni Finazzi
Paolo Longoni
Felix Kessler
Mutation of the Atypical Kinase ABC1K3 Partially Rescues the PROTON GRADIENT REGULATION 6 Phenotype in Arabidopsis thaliana
Frontiers in Plant Science
photosynthetic electron transport
plastoquinone pool
plastoglobule
high light acclimation
NPQ
author_facet Thibaut Pralon
Joy Collombat
Rosa Pipitone
Brigitte Ksas
Venkatasalam Shanmugabalaji
Michel Havaux
Giovanni Finazzi
Paolo Longoni
Felix Kessler
author_sort Thibaut Pralon
title Mutation of the Atypical Kinase ABC1K3 Partially Rescues the PROTON GRADIENT REGULATION 6 Phenotype in Arabidopsis thaliana
title_short Mutation of the Atypical Kinase ABC1K3 Partially Rescues the PROTON GRADIENT REGULATION 6 Phenotype in Arabidopsis thaliana
title_full Mutation of the Atypical Kinase ABC1K3 Partially Rescues the PROTON GRADIENT REGULATION 6 Phenotype in Arabidopsis thaliana
title_fullStr Mutation of the Atypical Kinase ABC1K3 Partially Rescues the PROTON GRADIENT REGULATION 6 Phenotype in Arabidopsis thaliana
title_full_unstemmed Mutation of the Atypical Kinase ABC1K3 Partially Rescues the PROTON GRADIENT REGULATION 6 Phenotype in Arabidopsis thaliana
title_sort mutation of the atypical kinase abc1k3 partially rescues the proton gradient regulation 6 phenotype in arabidopsis thaliana
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2020-03-01
description Photosynthesis is an essential pathway providing the chemical energy and reducing equivalents that sustain higher plant metabolism. It relies on sunlight, which is an inconstant source of energy that fluctuates in both intensity and spectrum. The fine and rapid tuning of the photosynthetic apparatus is essential to cope with changing light conditions and increase plant fitness. Recently PROTON GRADIENT REGULATION 6 (PGR6-ABC1K1), an atypical plastoglobule-associated kinase, was shown to regulate a new mechanism of light response by controlling the homeostasis of photoactive plastoquinone (PQ). PQ is a crucial electron carrier existing as a free neutral lipid in the photosynthetic thylakoid membrane. Perturbed homeostasis of PQ impairs photosynthesis and plant acclimation to high light. Here we show that a homologous kinase, ABC1K3, which like PGR6-ABC1K1 is associated with plastoglobules, also contributes to the homeostasis of the photoactive PQ pool. Contrary to PGR6-ABC1K1, ABC1K3 disfavors PQ availability for photosynthetic electron transport. In fact, in the abc1k1/abc1k3 double mutant the pgr6(abc1k1) the photosynthetic defect seen in the abc1k1 mutant is mitigated. However, the PQ concentration in the photoactive pool of the double mutant is comparable to that of abc1k1 mutant. An increase of the PQ mobility, inferred from the kinetics of its oxidation in dark, contributes to the mitigation of the pgr6(abc1k1) photosynthetic defect. Our results also demonstrate that ABC1K3 contributes to the regulation of other mechanisms involved in the adaptation of the photosynthetic apparatus to changes in light quality and intensity such as the induction of thermal dissipation and state transitions. Overall, we suggests that, besides the absolute concentration of PQ, its mobility and exchange between storage and active pools are critical for light acclimation in plants.
topic photosynthetic electron transport
plastoquinone pool
plastoglobule
high light acclimation
NPQ
url https://www.frontiersin.org/article/10.3389/fpls.2020.00337/full
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