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CRK2 and C-terminal phosphorylation of NADPH oxidase RBOHD regulate reactive oxygen species production in arabidopsis

Kimura, Sachie ; Hunter, Kerri ; Vaahtera, Lauri ; Tran, Huy Cuong LU orcid ; Citterico, Matteo ; Vaattovaara, Aleksia ; Rokka, Anne ; Stolze, Sara Christina ; Harzen, Anne and Meißner, Lena , et al. (2020) In Plant Cell 32(4). p.1063-1080
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... (More)

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.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
in
Plant Cell
volume
32
issue
4
pages
18 pages
publisher
American Society of Plant Biologists
external identifiers
  • scopus:85083082448
  • pmid:32034035
ISSN
1040-4651
DOI
10.1105/tpc.19.00525
language
English
LU publication?
yes
id
3179a313-2d95-4ca0-a2c1-dc09299235f1
date added to LUP
2020-12-18 14:15:30
date last changed
2024-06-28 06:37:36
@article{3179a313-2d95-4ca0-a2c1-dc09299235f1,
  abstract     = {{<p>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.</p>}},
  author       = {{Kimura, Sachie and Hunter, Kerri and Vaahtera, Lauri and Tran, Huy Cuong and Citterico, Matteo and Vaattovaara, Aleksia and Rokka, Anne and Stolze, Sara Christina and Harzen, Anne and Meißner, Lena and Wilkens, Maya Melina Tabea and Hamann, Thorsten and Toyota, Masatsugu and Nakagami, Hirofumi and Wrzaczek, Michael}},
  issn         = {{1040-4651}},
  language     = {{eng}},
  number       = {{4}},
  pages        = {{1063--1080}},
  publisher    = {{American Society of Plant Biologists}},
  series       = {{Plant Cell}},
  title        = {{CRK2 and C-terminal phosphorylation of NADPH oxidase RBOHD regulate reactive oxygen species production in arabidopsis}},
  url          = {{http://dx.doi.org/10.1105/tpc.19.00525}},
  doi          = {{10.1105/tpc.19.00525}},
  volume       = {{32}},
  year         = {{2020}},
}