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Comprehensive Identification of PTI Suppressors in Type III Effector Repertoire Reveals that Ralstonia solanacearum Activates Jasmonate Signaling at Two Different Steps

Ralstonia solanacearum is the causative agent of bacterial wilt in many plants. To identify R. solanacearum effectors that suppress pattern-triggered immunity (PTI) in plants, we transiently expressed R. solanacearum RS1000 effectors in Nicotiana benthamiana leaves and evaluated their ability to sup...

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Autores principales: Nakano, Masahito, Mukaihara, Takafumi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6928842/
https://www.ncbi.nlm.nih.gov/pubmed/31795135
http://dx.doi.org/10.3390/ijms20235992
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author Nakano, Masahito
Mukaihara, Takafumi
author_facet Nakano, Masahito
Mukaihara, Takafumi
author_sort Nakano, Masahito
collection PubMed
description Ralstonia solanacearum is the causative agent of bacterial wilt in many plants. To identify R. solanacearum effectors that suppress pattern-triggered immunity (PTI) in plants, we transiently expressed R. solanacearum RS1000 effectors in Nicotiana benthamiana leaves and evaluated their ability to suppress the production of reactive oxygen species (ROS) triggered by flg22. Out of the 61 effectors tested, 11 strongly and five moderately suppressed the flg22-triggered ROS burst. Among them, RipE1 shared homology with the Pseudomonas syringae cysteine protease effector HopX1. By yeast two-hybrid screening, we identified jasmonate-ZIM-domain (JAZ) proteins, which are transcriptional repressors of the jasmonic acid (JA) signaling pathway in plants, as RipE1 interactors. RipE1 promoted the degradation of JAZ repressors and induced the expressions of JA-responsive genes in a cysteine–protease-activity-dependent manner. Simultaneously, RipE1, similarly to the previously identified JA-producing effector RipAL, decreased the expression level of the salicylic acid synthesis gene that is required for the defense responses against R. solanacearum. The undecuple mutant that lacks 11 effectors with a strong PTI suppression activity showed reduced growth of R. solanacearum in Nicotiana plants. These results indicate that R. solanacearum subverts plant PTI responses using multiple effectors and manipulates JA signaling at two different steps to promote infection.
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spelling pubmed-69288422019-12-26 Comprehensive Identification of PTI Suppressors in Type III Effector Repertoire Reveals that Ralstonia solanacearum Activates Jasmonate Signaling at Two Different Steps Nakano, Masahito Mukaihara, Takafumi Int J Mol Sci Article Ralstonia solanacearum is the causative agent of bacterial wilt in many plants. To identify R. solanacearum effectors that suppress pattern-triggered immunity (PTI) in plants, we transiently expressed R. solanacearum RS1000 effectors in Nicotiana benthamiana leaves and evaluated their ability to suppress the production of reactive oxygen species (ROS) triggered by flg22. Out of the 61 effectors tested, 11 strongly and five moderately suppressed the flg22-triggered ROS burst. Among them, RipE1 shared homology with the Pseudomonas syringae cysteine protease effector HopX1. By yeast two-hybrid screening, we identified jasmonate-ZIM-domain (JAZ) proteins, which are transcriptional repressors of the jasmonic acid (JA) signaling pathway in plants, as RipE1 interactors. RipE1 promoted the degradation of JAZ repressors and induced the expressions of JA-responsive genes in a cysteine–protease-activity-dependent manner. Simultaneously, RipE1, similarly to the previously identified JA-producing effector RipAL, decreased the expression level of the salicylic acid synthesis gene that is required for the defense responses against R. solanacearum. The undecuple mutant that lacks 11 effectors with a strong PTI suppression activity showed reduced growth of R. solanacearum in Nicotiana plants. These results indicate that R. solanacearum subverts plant PTI responses using multiple effectors and manipulates JA signaling at two different steps to promote infection. MDPI 2019-11-28 /pmc/articles/PMC6928842/ /pubmed/31795135 http://dx.doi.org/10.3390/ijms20235992 Text en © 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Nakano, Masahito
Mukaihara, Takafumi
Comprehensive Identification of PTI Suppressors in Type III Effector Repertoire Reveals that Ralstonia solanacearum Activates Jasmonate Signaling at Two Different Steps
title Comprehensive Identification of PTI Suppressors in Type III Effector Repertoire Reveals that Ralstonia solanacearum Activates Jasmonate Signaling at Two Different Steps
title_full Comprehensive Identification of PTI Suppressors in Type III Effector Repertoire Reveals that Ralstonia solanacearum Activates Jasmonate Signaling at Two Different Steps
title_fullStr Comprehensive Identification of PTI Suppressors in Type III Effector Repertoire Reveals that Ralstonia solanacearum Activates Jasmonate Signaling at Two Different Steps
title_full_unstemmed Comprehensive Identification of PTI Suppressors in Type III Effector Repertoire Reveals that Ralstonia solanacearum Activates Jasmonate Signaling at Two Different Steps
title_short Comprehensive Identification of PTI Suppressors in Type III Effector Repertoire Reveals that Ralstonia solanacearum Activates Jasmonate Signaling at Two Different Steps
title_sort comprehensive identification of pti suppressors in type iii effector repertoire reveals that ralstonia solanacearum activates jasmonate signaling at two different steps
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6928842/
https://www.ncbi.nlm.nih.gov/pubmed/31795135
http://dx.doi.org/10.3390/ijms20235992
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