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The Orthotospovirus nonstructural protein NSs suppresses plant MYC-regulated jasmonate signaling leading to enhanced vector attraction and performance

Pandemics of vector-borne human and plant diseases often depend on the behaviors of their arthropod vectors. Arboviruses, including many bunyaviruses, manipulate vector behavior to accelerate their own transmission to vertebrates, birds, insects, and plants. However, the molecular mechanism underlyi...

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Autores principales: Wu, Xiujuan, Xu, Shuang, Zhao, Pingzhi, Zhang, Xuan, Yao, Xiangmei, Sun, Yanwei, Fang, Rongxiang, Ye, Jian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6598649/
https://www.ncbi.nlm.nih.gov/pubmed/31206553
http://dx.doi.org/10.1371/journal.ppat.1007897
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author Wu, Xiujuan
Xu, Shuang
Zhao, Pingzhi
Zhang, Xuan
Yao, Xiangmei
Sun, Yanwei
Fang, Rongxiang
Ye, Jian
author_facet Wu, Xiujuan
Xu, Shuang
Zhao, Pingzhi
Zhang, Xuan
Yao, Xiangmei
Sun, Yanwei
Fang, Rongxiang
Ye, Jian
author_sort Wu, Xiujuan
collection PubMed
description Pandemics of vector-borne human and plant diseases often depend on the behaviors of their arthropod vectors. Arboviruses, including many bunyaviruses, manipulate vector behavior to accelerate their own transmission to vertebrates, birds, insects, and plants. However, the molecular mechanism underlying this manipulation remains elusive. Here, we report that the non-structural protein NSs of Tomato spotted wilt orthotospovirus, a prototype of the Tospoviridae family and the Orthotospovirus genus, is a key viral factor that indirectly modifies vector preference and increases vector performance. NSs suppresses the biosynthesis of plant volatile monoterpenes, which serve as repellents of the vector western flower thrips (WFT, Frankliniella occidentalis). NSs directly interacts with MYC2, the jasmonate (JA) signaling master regulator and its two close homologs MYC3 and MYC4, to disable JA-mediated activation of terpene synthase genes. The dysfunction of the MYCs subsequently attenuates host defenses, increases the attraction of thrips, and improves thrips fitness. Moreover, MYC2 associated with NSs of Tomato zonate spot orthotospovirus, another Euro/Asian-type orthotospovirus, suggesting that MYC2 is an evolutionarily conserved target of Orthotospovirus species for suppression of terpene-based resistance to promote vector performance. These findings elucidate the molecular mechanism through which an orthotospovirus indirectly manipulates vector behaviors and therefore facilitates pathogen transmission. Our results provide insights into the molecular mechanisms by which Orthotospovirus NSs counteracts plant immunity for pathogen transmission.
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spelling pubmed-65986492019-07-05 The Orthotospovirus nonstructural protein NSs suppresses plant MYC-regulated jasmonate signaling leading to enhanced vector attraction and performance Wu, Xiujuan Xu, Shuang Zhao, Pingzhi Zhang, Xuan Yao, Xiangmei Sun, Yanwei Fang, Rongxiang Ye, Jian PLoS Pathog Research Article Pandemics of vector-borne human and plant diseases often depend on the behaviors of their arthropod vectors. Arboviruses, including many bunyaviruses, manipulate vector behavior to accelerate their own transmission to vertebrates, birds, insects, and plants. However, the molecular mechanism underlying this manipulation remains elusive. Here, we report that the non-structural protein NSs of Tomato spotted wilt orthotospovirus, a prototype of the Tospoviridae family and the Orthotospovirus genus, is a key viral factor that indirectly modifies vector preference and increases vector performance. NSs suppresses the biosynthesis of plant volatile monoterpenes, which serve as repellents of the vector western flower thrips (WFT, Frankliniella occidentalis). NSs directly interacts with MYC2, the jasmonate (JA) signaling master regulator and its two close homologs MYC3 and MYC4, to disable JA-mediated activation of terpene synthase genes. The dysfunction of the MYCs subsequently attenuates host defenses, increases the attraction of thrips, and improves thrips fitness. Moreover, MYC2 associated with NSs of Tomato zonate spot orthotospovirus, another Euro/Asian-type orthotospovirus, suggesting that MYC2 is an evolutionarily conserved target of Orthotospovirus species for suppression of terpene-based resistance to promote vector performance. These findings elucidate the molecular mechanism through which an orthotospovirus indirectly manipulates vector behaviors and therefore facilitates pathogen transmission. Our results provide insights into the molecular mechanisms by which Orthotospovirus NSs counteracts plant immunity for pathogen transmission. Public Library of Science 2019-06-17 /pmc/articles/PMC6598649/ /pubmed/31206553 http://dx.doi.org/10.1371/journal.ppat.1007897 Text en © 2019 Wu et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Wu, Xiujuan
Xu, Shuang
Zhao, Pingzhi
Zhang, Xuan
Yao, Xiangmei
Sun, Yanwei
Fang, Rongxiang
Ye, Jian
The Orthotospovirus nonstructural protein NSs suppresses plant MYC-regulated jasmonate signaling leading to enhanced vector attraction and performance
title The Orthotospovirus nonstructural protein NSs suppresses plant MYC-regulated jasmonate signaling leading to enhanced vector attraction and performance
title_full The Orthotospovirus nonstructural protein NSs suppresses plant MYC-regulated jasmonate signaling leading to enhanced vector attraction and performance
title_fullStr The Orthotospovirus nonstructural protein NSs suppresses plant MYC-regulated jasmonate signaling leading to enhanced vector attraction and performance
title_full_unstemmed The Orthotospovirus nonstructural protein NSs suppresses plant MYC-regulated jasmonate signaling leading to enhanced vector attraction and performance
title_short The Orthotospovirus nonstructural protein NSs suppresses plant MYC-regulated jasmonate signaling leading to enhanced vector attraction and performance
title_sort orthotospovirus nonstructural protein nss suppresses plant myc-regulated jasmonate signaling leading to enhanced vector attraction and performance
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6598649/
https://www.ncbi.nlm.nih.gov/pubmed/31206553
http://dx.doi.org/10.1371/journal.ppat.1007897
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