MAPK Signaling Regulates Nitric Oxide and NADPH Oxidase-Dependent Oxidative Bursts in Nicotiana benthamiana

Nitric oxide (NO) and reactive oxygen species (ROS) act as signals in innate immunity in plants. The radical burst is induced by INF1 elicitin, produced by the oomycete pathogen Phytophthora infestans. NO ASSOCIATED1 (NOA1) and NADPH oxidase participate in the radical burst. Here, we show that mitog...

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Published in:The Plant cell Vol. 20; no. 5; pp. 1390 - 1406
Main Authors: Asai, Shuta, Ohta, Kohji, Yoshioka, Hirofumi
Format: Journal Article
Language:English
Published: England American Society of Plant Biologists 01.05.2008
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ISSN:1040-4651, 1532-298X, 1532-298X
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Abstract Nitric oxide (NO) and reactive oxygen species (ROS) act as signals in innate immunity in plants. The radical burst is induced by INF1 elicitin, produced by the oomycete pathogen Phytophthora infestans. NO ASSOCIATED1 (NOA1) and NADPH oxidase participate in the radical burst. Here, we show that mitogen-activated protein kinase (MAPK) cascades MEK2-SIPK/NTF4 and MEK1-NTF6 participate in the regulation of the radical burst. NO generation was induced by conditional activation of SIPK/NTF4, but not by NTF6, in Nicotiana benthamiana leaves. INF1- and SIPK/NTF4-mediated NO bursts were compromised by the knockdown of NOA1. However, ROS generation was induced by either SIPK/NTF4 or NTF6. INF1- and MAPK-mediated ROS generation was eliminated by silencing Respiratory Burst Oxidase Homolog B (RBOHB), an inducible form of the NADPH oxidase. INF1-induced expression of RBOHB was compromised in SIPK/NTF4/NTF6-silenced leaves. These results indicated that INF1 regulates NOA1-mediated NO and RBOHB-dependent ROS generation through MAPK cascades. NOA1 silencing induced high susceptibility to Colletotrichum orbiculare but not to P. infestans; conversely, RBOHB silencing decreased resistance to P. infestans but not to C. orbiculare. These results indicate that the effects of the radical burst on the defense response appear to be diverse in plant-pathogen interactions.
AbstractList Nitric oxide (NO) and reactive oxygen species (ROS) act as signals in innate immunity in plants. The radical burst is induced by INF1 elicitin, produced by the oomycete pathogen Phytophthora infestans. NO ASSOCIATED1 (NOA1) and NADPH oxidase participate in the radical burst. Here, we show that mitogen-activated protein kinase (MAPK) cascades MEK2-SIPK/NTF4 and MEK1-NTF6 participate in the regulation of the radical burst. NO generation was induced by conditional activation of SIPK/NTF4, but not by NTF6, in Nicotiana benthamiana leaves. INF1- and SIPK/NTF4-mediated NO bursts were compromised by the knockdown of NOA1. However, ROS generation was induced by either SIPK/NTF4 or NTF6. INF1- and MAPK-mediated ROS generation was eliminated by silencing Respiratory Burst Oxidase Homolog B (RBOHB), an inducible form of the NADPH oxidase. INF1-induced expression of RBOHB was compromised in SIPK/NTF4/NTF6-silenced leaves. These results indicated that INF1 regulates NOA1-mediated NO and RBOHB-dependent ROS generation through MAPK cascades. NOA1 silencing induced high susceptibility to Colletotrichum orbiculare but not to P. infestans; conversely, RBOHB silencing decreased resistance to P. infestans but not to C. orbiculare. These results indicate that the effects of the radical burst on the defense response appear to be diverse in plant-pathogen interactions.
Nitric oxide (NO) and reactive oxygen species (ROS) act as signals in innate immunity in plants. The radical burst is induced by INF1 elicitin, produced by the oomycete pathogen Phytophthora infestans. NO ASSOCIATED1 (NOA1) and NADPH oxidase participate in the radical burst. Here, we show that mitogen-activated protein kinase (MAPK) cascades MEK2-SIPK/NTF4 and MEK1-NTF6 participate in the regulation of the radical burst. NO generation was induced by conditional activation of SIPK/NTF4, but not by NTF6, in Nicotiana benthamiana leaves. INF1- and SIPK/NTF4-mediated NO bursts were compromised by the knockdown of NOA1. However, ROS generation was induced by either SIPK/NTF4 or NTF6. INF1- and MAPK-mediated ROS generation was eliminated by silencing Respiratory Burst Oxidase Homolog B (RBOHB), an inducible form of the NADPH oxidase. INF1-induced expression of RBOHB was compromised in SIPK/NTF4/NTF6-silenced leaves. These results indicated that INF1 regulates NOA1-mediated NO and RBOHB-dependent ROS generation through MAPK cascades. NOA1 silencing induced high susceptibility to Colletotrichum orbiculare but not to P. infestans; conversely, RBOHB silencing decreased resistance to P. infestans but not to C. orbiculare. These results indicate that the effects of the radical burst on the defense response appear to be diverse in plant-pathogen interactions.Nitric oxide (NO) and reactive oxygen species (ROS) act as signals in innate immunity in plants. The radical burst is induced by INF1 elicitin, produced by the oomycete pathogen Phytophthora infestans. NO ASSOCIATED1 (NOA1) and NADPH oxidase participate in the radical burst. Here, we show that mitogen-activated protein kinase (MAPK) cascades MEK2-SIPK/NTF4 and MEK1-NTF6 participate in the regulation of the radical burst. NO generation was induced by conditional activation of SIPK/NTF4, but not by NTF6, in Nicotiana benthamiana leaves. INF1- and SIPK/NTF4-mediated NO bursts were compromised by the knockdown of NOA1. However, ROS generation was induced by either SIPK/NTF4 or NTF6. INF1- and MAPK-mediated ROS generation was eliminated by silencing Respiratory Burst Oxidase Homolog B (RBOHB), an inducible form of the NADPH oxidase. INF1-induced expression of RBOHB was compromised in SIPK/NTF4/NTF6-silenced leaves. These results indicated that INF1 regulates NOA1-mediated NO and RBOHB-dependent ROS generation through MAPK cascades. NOA1 silencing induced high susceptibility to Colletotrichum orbiculare but not to P. infestans; conversely, RBOHB silencing decreased resistance to P. infestans but not to C. orbiculare. These results indicate that the effects of the radical burst on the defense response appear to be diverse in plant-pathogen interactions.
Author Yoshioka, Hirofumi
Ohta, Kohji
Asai, Shuta
AuthorAffiliation b Plant Pathology Laboratory, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464-8601, Japan
a Laboratory of Defense in Plant–Pathogen Interactions, Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601, Japan
AuthorAffiliation_xml – name: a Laboratory of Defense in Plant–Pathogen Interactions, Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601, Japan
– name: b Plant Pathology Laboratory, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464-8601, Japan
Author_xml – sequence: 1
  fullname: Asai, Shuta
– sequence: 2
  fullname: Ohta, Kohji
– sequence: 3
  fullname: Yoshioka, Hirofumi
BackLink https://www.ncbi.nlm.nih.gov/pubmed/18515503$$D View this record in MEDLINE/PubMed
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Address correspondence to hyoshiok@agr.nagoya-u.ac.jp.
Online version contains Web-only data.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: Hirofumi Yoshioka (hyoshiok@agr.nagoya-u.ac.jp).
Open Access articles can be viewed online without a subscription.
www.plantcell.org/cgi/doi/10.1105/tpc.107.055855
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Snippet Nitric oxide (NO) and reactive oxygen species (ROS) act as signals in innate immunity in plants. The radical burst is induced by INF1 elicitin, produced by the...
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StartPage 1390
SubjectTerms Algal Proteins
Algal Proteins - pharmacology
Cell death
Colletotrichum
Colletotrichum - physiology
Colletotrichum orbiculare
drug effects
Gene expression regulation
genetics
Host-Pathogen Interactions
immunity
Immunoblotting
Inoculation
Leaves
MAP Kinase Kinase 2
MAP Kinase Kinase 2 - genetics
MAP Kinase Kinase 2 - metabolism
MAP Kinase Signaling System
MAP Kinase Signaling System - drug effects
MAP Kinase Signaling System - genetics
MAP Kinase Signaling System - physiology
metabolism
microbiology
mitogen-activated protein kinase
Mitogen-Activated Protein Kinases
Mitogen-Activated Protein Kinases - genetics
Mitogen-Activated Protein Kinases - metabolism
Molecular Sequence Data
Mutagenesis, Site-Directed
NADP (coenzyme)
NADPH Oxidases
NADPH Oxidases - genetics
NADPH Oxidases - metabolism
Nicotiana - genetics
Nicotiana - metabolism
Nicotiana - microbiology
Nicotiana benthamiana
Nitric oxide
Nitric Oxide - metabolism
Nitric Oxide Synthase
Nitric Oxide Synthase - genetics
Nitric Oxide Synthase - metabolism
Oomycetes
Oxidases
Oxides
Pathogens
pharmacology
physiology
Phytophthora
Phytophthora - physiology
Phytophthora infestans
Plant cells
Plant Proteins
Plant Proteins - genetics
Plant Proteins - metabolism
Plant Proteins - physiology
Plants
Proteins
Reactive oxygen species
Reactive Oxygen Species - metabolism
Reverse Transcriptase Polymerase Chain Reaction
Tobacco
Title MAPK Signaling Regulates Nitric Oxide and NADPH Oxidase-Dependent Oxidative Bursts in Nicotiana benthamiana
URI https://www.jstor.org/stable/25224245
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Volume 20
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