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Research ArticleResearch Article
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CRK2 and C-terminal Phosphorylation of NADPH Oxidase RBOHD Regulate Reactive Oxygen Species Production in Arabidopsis

Sachie Kimura, Kerri Hunter, Lauri Vaahtera, Huy Cuong Tran, Matteo Citterico, Aleksia Vaattovaara, Anne Rokka, Sara Christina Stolze, Anne Harzen, Lena Meißner, Maya Melina Tabea Wilkens, Thorsten Hamann, Masatsugu Toyota, Hirofumi Nakagami, Michael Wrzaczek
Sachie Kimura
aOrganismal and Evolutionary Biology Research Programme, Viikki Plant Science Centre, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki FI-00014, Finland
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  • ORCID record for Sachie Kimura
Kerri Hunter
aOrganismal and Evolutionary Biology Research Programme, Viikki Plant Science Centre, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki FI-00014, Finland
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Lauri Vaahtera
bDepartment of Biology, Norwegian University of Science and Technology, 7491 Trondheim, Norway
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  • ORCID record for Lauri Vaahtera
Huy Cuong Tran
aOrganismal and Evolutionary Biology Research Programme, Viikki Plant Science Centre, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki FI-00014, Finland
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Matteo Citterico
aOrganismal and Evolutionary Biology Research Programme, Viikki Plant Science Centre, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki FI-00014, Finland
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Aleksia Vaattovaara
aOrganismal and Evolutionary Biology Research Programme, Viikki Plant Science Centre, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki FI-00014, Finland
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Anne Rokka
cTurku Centre for Biotechnology, University of Turku and Åbo Akademi University, Turku FI-20520, Finland
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Sara Christina Stolze
dProtein Mass Spectrometry Group, Max-Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany
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Anne Harzen
dProtein Mass Spectrometry Group, Max-Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany
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Lena Meißner
aOrganismal and Evolutionary Biology Research Programme, Viikki Plant Science Centre, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki FI-00014, Finland
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  • ORCID record for Lena Meißner
Maya Melina Tabea Wilkens
aOrganismal and Evolutionary Biology Research Programme, Viikki Plant Science Centre, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki FI-00014, Finland
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Thorsten Hamann
bDepartment of Biology, Norwegian University of Science and Technology, 7491 Trondheim, Norway
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Masatsugu Toyota
eDepartment of Biochemistry and Molecular Biology, Saitama University, Saitama 338-8570, Japan
fDepartment of Botany, University of Wisconsin, Madison, WI 53593, USA
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Hirofumi Nakagami
dProtein Mass Spectrometry Group, Max-Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany
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Michael Wrzaczek
aOrganismal and Evolutionary Biology Research Programme, Viikki Plant Science Centre, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki FI-00014, Finland
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  • For correspondence: michael.wrzaczek@helsinki.fi

Published April 2020. DOI: https://doi.org/10.1105/tpc.19.00525

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  • © 2020 American Society of Plant Biologists. All rights reserved.

Abstract

Reactive oxygen species (ROS) are important messengers in eukaryotic organisms, and their production is tightly controlled. Active extracellular ROS production by NADPH oxidases in plants is triggered by receptor-like protein kinase-dependent signaling networks. Here, we show that CYSTEINE-RICH RLK2 (CRK2) kinase activity is required for plant growth and CRK2 exists in a preformed complex with the NADPH oxidase RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD) in Arabidopsis (Arabidopsis thaliana). Functional CRK2 is required for the full elicitor-induced ROS burst, and consequently the crk2 mutant is impaired in defense against the bacterial pathogen Pseudomonas syringae pv tomato DC3000. Our work demonstrates that CRK2 regulates plant innate immunity. We identified in vitro CRK2-dependent phosphorylation sites in the C-terminal region of RBOHD. Phosphorylation of S703 RBOHD is enhanced upon flg22 treatment, and substitution of S703 with Ala reduced ROS production in Arabidopsis. Phylogenetic analysis suggests that phospho-sites in the C-terminal region of RBOHD are conserved throughout the plant lineage and between animals and plants. We propose that regulation of NADPH oxidase activity by phosphorylation of the C-terminal region might be an ancient mechanism and that CRK2 is an important element in regulating microbe-associated molecular pattern-triggered ROS production.

  • Received July 12, 2019.
  • Revised January 13, 2020.
  • Accepted February 6, 2020.
  • Published February 7, 2020.

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CRK2 and C-terminal Phosphorylation of NADPH Oxidase RBOHD Regulate Reactive Oxygen Species Production in Arabidopsis
Sachie Kimura, Kerri Hunter, Lauri Vaahtera, Huy Cuong Tran, Matteo Citterico, Aleksia Vaattovaara, Anne Rokka, Sara Christina Stolze, Anne Harzen, Lena Meißner, Maya Melina Tabea Wilkens, Thorsten Hamann, Masatsugu Toyota, Hirofumi Nakagami, Michael Wrzaczek
The Plant Cell Apr 2020, 32 (4) 1063-1080; DOI: 10.1105/tpc.19.00525

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CRK2 and C-terminal Phosphorylation of NADPH Oxidase RBOHD Regulate Reactive Oxygen Species Production in Arabidopsis
Sachie Kimura, Kerri Hunter, Lauri Vaahtera, Huy Cuong Tran, Matteo Citterico, Aleksia Vaattovaara, Anne Rokka, Sara Christina Stolze, Anne Harzen, Lena Meißner, Maya Melina Tabea Wilkens, Thorsten Hamann, Masatsugu Toyota, Hirofumi Nakagami, Michael Wrzaczek
The Plant Cell Apr 2020, 32 (4) 1063-1080; DOI: 10.1105/tpc.19.00525
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  • Peer Review Report
  • IN BRIEF: En Garde: CRK2 Pre-associates with RBOHD and Regulates ROS Production
  • First author profile: Sachie Kimura

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The Plant Cell: 32 (4)
The Plant Cell
Vol. 32, Issue 4
Apr 2020
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