Ustilago maydis effector Jsi1 interacts with Topless corepressor, hijacking plant jasmonate/ethylene signaling
• Ustilago maydis is the causal agent of maize smut disease. During the colonization process, the fungus secretes effector proteins that suppress immune responses and redirect the host metabolism in favor of the pathogen. As effectors play a critical role during plant colonization, their identificat...
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| Veröffentlicht in: | The New phytologist 2021-03, Vol.229 (6), p.3393-3407 |
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| creator | Darino, Martin Chia, Khong-Sam Marques, Joana Aleksza, David Soto-Jiménez, Luz Mayela Saado, Indira Uhse, Simon Borg, Michael Betz, Ruben Bindics, Janos Zienkiewicz, Krzysztof Feussner, Ivo Petit-Houdenot, Yohann Djamei, Armin |
| description | • Ustilago maydis is the causal agent of maize smut disease. During the colonization process, the fungus secretes effector proteins that suppress immune responses and redirect the host metabolism in favor of the pathogen. As effectors play a critical role during plant colonization, their identification and functional characterization are essential to understanding biotrophy and disease.
• Using biochemical, molecular, and transcriptomic techniques, we performed a functional characterization of the U. maydis effector Jasmonate/Ethylene signaling inducer 1 (Jsi1).
• Jsi1 interacts with several members of the plant corepressor family Topless/Topless related (TPL/TPR). Jsi1 expression in Zea mays and Arabidopsis thaliana leads to transcriptional induction of the ethylene response factor (ERF) branch of the jasmonate/ethylene (JA/ET) signaling pathway. In A. thaliana, activation of the ERF branch leads to biotrophic susceptibility. Jsi1 likely activates the ERF branch via an EAR (ET-responsive element binding-factor-associated amphiphilic repression) motif, which resembles EAR motifs from plant ERF transcription factors, that interacts with TPL/TPR proteins.
• EAR-motif-containing effector candidates were identified from different fungal species, including Magnaporthe oryzae, Sporisorium scitamineum, and Sporisorium reilianum. Interaction between plant TPL proteins and these effector candidates from biotrophic and hemibiotrophic fungi indicates the convergent evolution of effectors modulating the TPL/TPR corepressor hub. |
| doi_str_mv | 10.1111/nph.17116 |
| format | Article |
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• Using biochemical, molecular, and transcriptomic techniques, we performed a functional characterization of the U. maydis effector Jasmonate/Ethylene signaling inducer 1 (Jsi1).
• Jsi1 interacts with several members of the plant corepressor family Topless/Topless related (TPL/TPR). Jsi1 expression in Zea mays and Arabidopsis thaliana leads to transcriptional induction of the ethylene response factor (ERF) branch of the jasmonate/ethylene (JA/ET) signaling pathway. In A. thaliana, activation of the ERF branch leads to biotrophic susceptibility. Jsi1 likely activates the ERF branch via an EAR (ET-responsive element binding-factor-associated amphiphilic repression) motif, which resembles EAR motifs from plant ERF transcription factors, that interacts with TPL/TPR proteins.
• EAR-motif-containing effector candidates were identified from different fungal species, including Magnaporthe oryzae, Sporisorium scitamineum, and Sporisorium reilianum. Interaction between plant TPL proteins and these effector candidates from biotrophic and hemibiotrophic fungi indicates the convergent evolution of effectors modulating the TPL/TPR corepressor hub.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.17116</identifier><identifier>PMID: 33247447</identifier><language>eng</language><publisher>England: Wiley</publisher><subject>Ascomycota ; Basidiomycota ; Co-Repressor Proteins ; Colonization ; Cyclopentanes ; EAR motif ; Effectors ; Ethene ; Ethylene ; ethylene response factor ; Ethylenes ; Fungal Proteins ; Fungi ; Immune response ; jasmonate/ethylene (JA/ET) signaling ; Jasmonic acid ; Jsi1 ; Life Sciences ; Metabolism ; Oxylipins ; Pathogens ; Plant Diseases ; Proteins ; Regulatory sequences ; Signal transduction ; Signaling ; Smut ; Topless ; Transcription ; Transcription factors ; Ustilago ; Ustilago maydis ; Zea mays</subject><ispartof>The New phytologist, 2021-03, Vol.229 (6), p.3393-3407</ispartof><rights>2020 The Authors © 2020 New Phytologist Foundation</rights><rights>2020 The Authors New Phytologist © 2020 New Phytologist Foundation</rights><rights>2020 The Authors New Phytologist © 2020 New Phytologist Foundation.</rights><rights>2020. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Attribution</rights><rights>2020 The Authors. © 2020 New Phytologist Foundation</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4996-130370d6dfcd62c91f7f6db51dc800f1b345309d4a3f728d5d8bad8132031cdd3</citedby><cites>FETCH-LOGICAL-c4996-130370d6dfcd62c91f7f6db51dc800f1b345309d4a3f728d5d8bad8132031cdd3</cites><orcidid>0000-0002-4995-795X ; 0000-0003-4806-8349 ; 0000-0002-8922-3969 ; 0000-0002-3982-3843 ; 0000-0002-4597-535X ; 0000-0002-7449-220X ; 0000-0002-3462-0983 ; 0000-0002-8525-9569 ; 0000-0002-8087-9566 ; 0000-0003-0190-5314 ; 0000-0002-9888-7003</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fnph.17116$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.17116$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33247447$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-03121717$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Darino, Martin</creatorcontrib><creatorcontrib>Chia, Khong-Sam</creatorcontrib><creatorcontrib>Marques, Joana</creatorcontrib><creatorcontrib>Aleksza, David</creatorcontrib><creatorcontrib>Soto-Jiménez, Luz Mayela</creatorcontrib><creatorcontrib>Saado, Indira</creatorcontrib><creatorcontrib>Uhse, Simon</creatorcontrib><creatorcontrib>Borg, Michael</creatorcontrib><creatorcontrib>Betz, Ruben</creatorcontrib><creatorcontrib>Bindics, Janos</creatorcontrib><creatorcontrib>Zienkiewicz, Krzysztof</creatorcontrib><creatorcontrib>Feussner, Ivo</creatorcontrib><creatorcontrib>Petit-Houdenot, Yohann</creatorcontrib><creatorcontrib>Djamei, Armin</creatorcontrib><title>Ustilago maydis effector Jsi1 interacts with Topless corepressor, hijacking plant jasmonate/ethylene signaling</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>• Ustilago maydis is the causal agent of maize smut disease. During the colonization process, the fungus secretes effector proteins that suppress immune responses and redirect the host metabolism in favor of the pathogen. As effectors play a critical role during plant colonization, their identification and functional characterization are essential to understanding biotrophy and disease.
• Using biochemical, molecular, and transcriptomic techniques, we performed a functional characterization of the U. maydis effector Jasmonate/Ethylene signaling inducer 1 (Jsi1).
• Jsi1 interacts with several members of the plant corepressor family Topless/Topless related (TPL/TPR). Jsi1 expression in Zea mays and Arabidopsis thaliana leads to transcriptional induction of the ethylene response factor (ERF) branch of the jasmonate/ethylene (JA/ET) signaling pathway. In A. thaliana, activation of the ERF branch leads to biotrophic susceptibility. Jsi1 likely activates the ERF branch via an EAR (ET-responsive element binding-factor-associated amphiphilic repression) motif, which resembles EAR motifs from plant ERF transcription factors, that interacts with TPL/TPR proteins.
• EAR-motif-containing effector candidates were identified from different fungal species, including Magnaporthe oryzae, Sporisorium scitamineum, and Sporisorium reilianum. Interaction between plant TPL proteins and these effector candidates from biotrophic and hemibiotrophic fungi indicates the convergent evolution of effectors modulating the TPL/TPR corepressor hub.</description><subject>Ascomycota</subject><subject>Basidiomycota</subject><subject>Co-Repressor Proteins</subject><subject>Colonization</subject><subject>Cyclopentanes</subject><subject>EAR motif</subject><subject>Effectors</subject><subject>Ethene</subject><subject>Ethylene</subject><subject>ethylene response factor</subject><subject>Ethylenes</subject><subject>Fungal Proteins</subject><subject>Fungi</subject><subject>Immune response</subject><subject>jasmonate/ethylene (JA/ET) signaling</subject><subject>Jasmonic acid</subject><subject>Jsi1</subject><subject>Life Sciences</subject><subject>Metabolism</subject><subject>Oxylipins</subject><subject>Pathogens</subject><subject>Plant Diseases</subject><subject>Proteins</subject><subject>Regulatory sequences</subject><subject>Signal transduction</subject><subject>Signaling</subject><subject>Smut</subject><subject>Topless</subject><subject>Transcription</subject><subject>Transcription factors</subject><subject>Ustilago</subject><subject>Ustilago maydis</subject><subject>Zea mays</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNp1kk1v0zAYxy0EYqVw4AOALHEBiax-ixNfkKaJUVAFHDaJm-XaTuOQ2MFON_Xbz6VbgUn4Ysv-Pf_n5W8AXmJ0ivNa-LE9xRXG_BGYYcZFUWNaPQYzhEhdcMZ_nIBnKXUIIVFy8hScUEpYxVg1A_4qTa5XmwAHtTMuQds0Vk8hwi_JYej8ZKPSU4I3bmrhZRh7mxLUIdox5lOI72HrOqV_Or-BY6_8BDuVhuDVZBd2ane99RYmt_Gqz8hz8KRRfbIv7vY5uLr4eHm-LFbfPn0-P1sVmgnBC0wRrZDhptGGEy1wUzXcrEtsdI1Qg9eUlRQJwxRtKlKb0tRrZXLXBFGsjaFz8OGgO27XgzXa-imqXo7RDSruZFBO_vviXSs34VrWmHBRiizw7iDQPghbnq3k_i4nInnm1TXO7Nu7ZDH82to0ycElbfs8DRu2SRLGS0ZLkmuegzcP0C5sY57NnhLZoJrT8k9yHUNK0TbHCjCSe8dldlz-djyzr__u9EjeW5yBxQG4cb3d_V9Jfv2-vJd8dYjoUv4IxwhSIZSNEfQWT2rAcg</recordid><startdate>202103</startdate><enddate>202103</enddate><creator>Darino, Martin</creator><creator>Chia, Khong-Sam</creator><creator>Marques, Joana</creator><creator>Aleksza, David</creator><creator>Soto-Jiménez, Luz Mayela</creator><creator>Saado, Indira</creator><creator>Uhse, Simon</creator><creator>Borg, Michael</creator><creator>Betz, Ruben</creator><creator>Bindics, Janos</creator><creator>Zienkiewicz, Krzysztof</creator><creator>Feussner, Ivo</creator><creator>Petit-Houdenot, Yohann</creator><creator>Djamei, Armin</creator><general>Wiley</general><general>Wiley Subscription Services, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4995-795X</orcidid><orcidid>https://orcid.org/0000-0003-4806-8349</orcidid><orcidid>https://orcid.org/0000-0002-8922-3969</orcidid><orcidid>https://orcid.org/0000-0002-3982-3843</orcidid><orcidid>https://orcid.org/0000-0002-4597-535X</orcidid><orcidid>https://orcid.org/0000-0002-7449-220X</orcidid><orcidid>https://orcid.org/0000-0002-3462-0983</orcidid><orcidid>https://orcid.org/0000-0002-8525-9569</orcidid><orcidid>https://orcid.org/0000-0002-8087-9566</orcidid><orcidid>https://orcid.org/0000-0003-0190-5314</orcidid><orcidid>https://orcid.org/0000-0002-9888-7003</orcidid></search><sort><creationdate>202103</creationdate><title>Ustilago maydis effector Jsi1 interacts with Topless corepressor, hijacking plant jasmonate/ethylene signaling</title><author>Darino, Martin ; Chia, Khong-Sam ; Marques, Joana ; Aleksza, David ; Soto-Jiménez, Luz Mayela ; Saado, Indira ; Uhse, Simon ; Borg, Michael ; Betz, Ruben ; Bindics, Janos ; Zienkiewicz, Krzysztof ; Feussner, Ivo ; Petit-Houdenot, Yohann ; Djamei, Armin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4996-130370d6dfcd62c91f7f6db51dc800f1b345309d4a3f728d5d8bad8132031cdd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Ascomycota</topic><topic>Basidiomycota</topic><topic>Co-Repressor Proteins</topic><topic>Colonization</topic><topic>Cyclopentanes</topic><topic>EAR motif</topic><topic>Effectors</topic><topic>Ethene</topic><topic>Ethylene</topic><topic>ethylene response factor</topic><topic>Ethylenes</topic><topic>Fungal Proteins</topic><topic>Fungi</topic><topic>Immune response</topic><topic>jasmonate/ethylene (JA/ET) signaling</topic><topic>Jasmonic acid</topic><topic>Jsi1</topic><topic>Life Sciences</topic><topic>Metabolism</topic><topic>Oxylipins</topic><topic>Pathogens</topic><topic>Plant Diseases</topic><topic>Proteins</topic><topic>Regulatory sequences</topic><topic>Signal transduction</topic><topic>Signaling</topic><topic>Smut</topic><topic>Topless</topic><topic>Transcription</topic><topic>Transcription factors</topic><topic>Ustilago</topic><topic>Ustilago maydis</topic><topic>Zea mays</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Darino, Martin</creatorcontrib><creatorcontrib>Chia, Khong-Sam</creatorcontrib><creatorcontrib>Marques, Joana</creatorcontrib><creatorcontrib>Aleksza, David</creatorcontrib><creatorcontrib>Soto-Jiménez, Luz Mayela</creatorcontrib><creatorcontrib>Saado, Indira</creatorcontrib><creatorcontrib>Uhse, Simon</creatorcontrib><creatorcontrib>Borg, Michael</creatorcontrib><creatorcontrib>Betz, Ruben</creatorcontrib><creatorcontrib>Bindics, Janos</creatorcontrib><creatorcontrib>Zienkiewicz, Krzysztof</creatorcontrib><creatorcontrib>Feussner, Ivo</creatorcontrib><creatorcontrib>Petit-Houdenot, Yohann</creatorcontrib><creatorcontrib>Djamei, Armin</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Darino, Martin</au><au>Chia, Khong-Sam</au><au>Marques, Joana</au><au>Aleksza, David</au><au>Soto-Jiménez, Luz Mayela</au><au>Saado, Indira</au><au>Uhse, Simon</au><au>Borg, Michael</au><au>Betz, Ruben</au><au>Bindics, Janos</au><au>Zienkiewicz, Krzysztof</au><au>Feussner, Ivo</au><au>Petit-Houdenot, Yohann</au><au>Djamei, Armin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ustilago maydis effector Jsi1 interacts with Topless corepressor, hijacking plant jasmonate/ethylene signaling</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2021-03</date><risdate>2021</risdate><volume>229</volume><issue>6</issue><spage>3393</spage><epage>3407</epage><pages>3393-3407</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>• Ustilago maydis is the causal agent of maize smut disease. During the colonization process, the fungus secretes effector proteins that suppress immune responses and redirect the host metabolism in favor of the pathogen. As effectors play a critical role during plant colonization, their identification and functional characterization are essential to understanding biotrophy and disease.
• Using biochemical, molecular, and transcriptomic techniques, we performed a functional characterization of the U. maydis effector Jasmonate/Ethylene signaling inducer 1 (Jsi1).
• Jsi1 interacts with several members of the plant corepressor family Topless/Topless related (TPL/TPR). Jsi1 expression in Zea mays and Arabidopsis thaliana leads to transcriptional induction of the ethylene response factor (ERF) branch of the jasmonate/ethylene (JA/ET) signaling pathway. In A. thaliana, activation of the ERF branch leads to biotrophic susceptibility. Jsi1 likely activates the ERF branch via an EAR (ET-responsive element binding-factor-associated amphiphilic repression) motif, which resembles EAR motifs from plant ERF transcription factors, that interacts with TPL/TPR proteins.
• EAR-motif-containing effector candidates were identified from different fungal species, including Magnaporthe oryzae, Sporisorium scitamineum, and Sporisorium reilianum. Interaction between plant TPL proteins and these effector candidates from biotrophic and hemibiotrophic fungi indicates the convergent evolution of effectors modulating the TPL/TPR corepressor hub.</abstract><cop>England</cop><pub>Wiley</pub><pmid>33247447</pmid><doi>10.1111/nph.17116</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-4995-795X</orcidid><orcidid>https://orcid.org/0000-0003-4806-8349</orcidid><orcidid>https://orcid.org/0000-0002-8922-3969</orcidid><orcidid>https://orcid.org/0000-0002-3982-3843</orcidid><orcidid>https://orcid.org/0000-0002-4597-535X</orcidid><orcidid>https://orcid.org/0000-0002-7449-220X</orcidid><orcidid>https://orcid.org/0000-0002-3462-0983</orcidid><orcidid>https://orcid.org/0000-0002-8525-9569</orcidid><orcidid>https://orcid.org/0000-0002-8087-9566</orcidid><orcidid>https://orcid.org/0000-0003-0190-5314</orcidid><orcidid>https://orcid.org/0000-0002-9888-7003</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | The New phytologist, 2021-03, Vol.229 (6), p.3393-3407 |
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| source | MEDLINE; Wiley Online Library Journals Frontfile Complete; Wiley Online Library Free Content; EZB-FREE-00999 freely available EZB journals |
| subjects | Ascomycota Basidiomycota Co-Repressor Proteins Colonization Cyclopentanes EAR motif Effectors Ethene Ethylene ethylene response factor Ethylenes Fungal Proteins Fungi Immune response jasmonate/ethylene (JA/ET) signaling Jasmonic acid Jsi1 Life Sciences Metabolism Oxylipins Pathogens Plant Diseases Proteins Regulatory sequences Signal transduction Signaling Smut Topless Transcription Transcription factors Ustilago Ustilago maydis Zea mays |
| title | Ustilago maydis effector Jsi1 interacts with Topless corepressor, hijacking plant jasmonate/ethylene signaling |
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