Selective deployment of virulence effectors correlates with host specificity in a fungal plant pathogen
Summary The hemibiotrophic fungal plant pathogen Colletotrichum orbiculare is predicted to secrete hundreds of effector proteins when the pathogen infects cucurbit crops, such as cucumber and melon, and tobacco (Nicotiana benthamiana), a distantly related Solanaceae species. Here, we report the iden...
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| Veröffentlicht in: | The New phytologist 2023-05, Vol.238 (4), p.1578-1592 |
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| container_title | The New phytologist |
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| creator | Inoue, Yoshihiro Phuong Vy, Trinh Thi Singkaravanit‐Ogawa, Suthitar Zhang, Ru Yamada, Kohji Ogawa, Taiki Ishizuka, Junya Narusaka, Yoshihiro Takano, Yoshitaka |
| description | Summary
The hemibiotrophic fungal plant pathogen Colletotrichum orbiculare is predicted to secrete hundreds of effector proteins when the pathogen infects cucurbit crops, such as cucumber and melon, and tobacco (Nicotiana benthamiana), a distantly related Solanaceae species. Here, we report the identification of sets of C. orbiculare effector genes that are differentially required for fungal virulence to two phylogenetically distant host species.
Through targeted gene knockout screening of C. orbiculare ‘core’ effector candidates defined based on in planta gene expression, we identified: four host‐specific virulence effectors (named effector proteins for cucurbit infection, or EPCs) that are required for full virulence of C. orbiculare to cucurbit hosts, but not to the Solanaceae host N. benthamiana; and five host‐nonspecific virulence effectors, which collectively contribute to fungal virulence to both hosts.
During host infection, only a small subset of genes, including the host‐specific EPC effector genes, showed preferential expression on one of the hosts, while gene expression profiles of the majority of other genes, including the five host‐nonspecific effector genes, were common to both hosts.
This work suggests that C. orbiculare adopts a host‐specific effector deployment strategy, in addition to general host‐blind virulence mechanisms, for adaptation to cucurbit hosts. |
| doi_str_mv | 10.1111/nph.18790 |
| format | Article |
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The hemibiotrophic fungal plant pathogen Colletotrichum orbiculare is predicted to secrete hundreds of effector proteins when the pathogen infects cucurbit crops, such as cucumber and melon, and tobacco (Nicotiana benthamiana), a distantly related Solanaceae species. Here, we report the identification of sets of C. orbiculare effector genes that are differentially required for fungal virulence to two phylogenetically distant host species.
Through targeted gene knockout screening of C. orbiculare ‘core’ effector candidates defined based on in planta gene expression, we identified: four host‐specific virulence effectors (named effector proteins for cucurbit infection, or EPCs) that are required for full virulence of C. orbiculare to cucurbit hosts, but not to the Solanaceae host N. benthamiana; and five host‐nonspecific virulence effectors, which collectively contribute to fungal virulence to both hosts.
During host infection, only a small subset of genes, including the host‐specific EPC effector genes, showed preferential expression on one of the hosts, while gene expression profiles of the majority of other genes, including the five host‐nonspecific effector genes, were common to both hosts.
This work suggests that C. orbiculare adopts a host‐specific effector deployment strategy, in addition to general host‐blind virulence mechanisms, for adaptation to cucurbit hosts.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.18790</identifier><identifier>PMID: 36939621</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Colletotrichum orbiculare ; Cucumis sativus - microbiology ; Cucurbitaceae - genetics ; Cucurbitaceae - metabolism ; Cucurbitaceae - microbiology ; Deployment ; Effectors ; Fungal Proteins - genetics ; Fungal Proteins - metabolism ; Fungi ; Gene expression ; Genes ; Host Specificity ; Hosts ; Nicotiana - genetics ; Nicotiana benthamiana ; Pathogens ; Phylogeny ; phytopathogenic fungi ; Plant Diseases - microbiology ; Proteins ; Secretion ; Solanaceae ; Specificity ; Tobacco ; transcriptional control ; Transcriptome ; Virulence ; Virulence - genetics ; virulence effector</subject><ispartof>The New phytologist, 2023-05, Vol.238 (4), p.1578-1592</ispartof><rights>2023 The Authors. © 2023 New Phytologist Foundation</rights><rights>2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.</rights><rights>2023. 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><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4980-987f0b69c59f2a277e4a95b0fe863775ed243b9a892fae75527eb7bcfc41f06f3</citedby><cites>FETCH-LOGICAL-c4980-987f0b69c59f2a277e4a95b0fe863775ed243b9a892fae75527eb7bcfc41f06f3</cites><orcidid>0000-0002-0353-1726 ; 0000-0003-1427-1322</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.18790$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.18790$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36939621$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Inoue, Yoshihiro</creatorcontrib><creatorcontrib>Phuong Vy, Trinh Thi</creatorcontrib><creatorcontrib>Singkaravanit‐Ogawa, Suthitar</creatorcontrib><creatorcontrib>Zhang, Ru</creatorcontrib><creatorcontrib>Yamada, Kohji</creatorcontrib><creatorcontrib>Ogawa, Taiki</creatorcontrib><creatorcontrib>Ishizuka, Junya</creatorcontrib><creatorcontrib>Narusaka, Yoshihiro</creatorcontrib><creatorcontrib>Takano, Yoshitaka</creatorcontrib><title>Selective deployment of virulence effectors correlates with host specificity in a fungal plant pathogen</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
The hemibiotrophic fungal plant pathogen Colletotrichum orbiculare is predicted to secrete hundreds of effector proteins when the pathogen infects cucurbit crops, such as cucumber and melon, and tobacco (Nicotiana benthamiana), a distantly related Solanaceae species. Here, we report the identification of sets of C. orbiculare effector genes that are differentially required for fungal virulence to two phylogenetically distant host species.
Through targeted gene knockout screening of C. orbiculare ‘core’ effector candidates defined based on in planta gene expression, we identified: four host‐specific virulence effectors (named effector proteins for cucurbit infection, or EPCs) that are required for full virulence of C. orbiculare to cucurbit hosts, but not to the Solanaceae host N. benthamiana; and five host‐nonspecific virulence effectors, which collectively contribute to fungal virulence to both hosts.
During host infection, only a small subset of genes, including the host‐specific EPC effector genes, showed preferential expression on one of the hosts, while gene expression profiles of the majority of other genes, including the five host‐nonspecific effector genes, were common to both hosts.
This work suggests that C. orbiculare adopts a host‐specific effector deployment strategy, in addition to general host‐blind virulence mechanisms, for adaptation to cucurbit hosts.</description><subject>Colletotrichum orbiculare</subject><subject>Cucumis sativus - microbiology</subject><subject>Cucurbitaceae - genetics</subject><subject>Cucurbitaceae - metabolism</subject><subject>Cucurbitaceae - microbiology</subject><subject>Deployment</subject><subject>Effectors</subject><subject>Fungal Proteins - genetics</subject><subject>Fungal Proteins - metabolism</subject><subject>Fungi</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Host Specificity</subject><subject>Hosts</subject><subject>Nicotiana - genetics</subject><subject>Nicotiana benthamiana</subject><subject>Pathogens</subject><subject>Phylogeny</subject><subject>phytopathogenic fungi</subject><subject>Plant Diseases - microbiology</subject><subject>Proteins</subject><subject>Secretion</subject><subject>Solanaceae</subject><subject>Specificity</subject><subject>Tobacco</subject><subject>transcriptional control</subject><subject>Transcriptome</subject><subject>Virulence</subject><subject>Virulence - genetics</subject><subject>virulence effector</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNp10M1LwzAYx_Egis6Xg_-ABLzooS5J26Q5yvANRAUVvJU0e7JFsqYmrWP_vdGpB8Fccvnw5eGH0CElZzS9cdvNz2glJNlAI1pwmVU0F5toRAirMl7wlx20G-MrIUSWnG2jnZzLXHJGR2j2CA50b98BT6FzfrWAtsfe4HcbBgetBgzGJOFDxNqHAE71EPHS9nM897HHsQNtjdW2X2HbYoXN0M6Uw51TqdSpfu5n0O6jLaNchIPvfw89X148Ta6z2_urm8n5baYLWZFMVsKQhktdSsMUEwIKJcuGGKh4LkQJU1bkjVSVZEaBKEsmoBGNNrqghnCT76GTdbcL_m2A2NcLGzW4dAz4IdZMVGkozvIy0eM_9NUPoU3XJSWlFJyWRVKna6WDjzGAqbtgFyqsakrqz_XrtH79tX6yR9_FoVnA9Ff-zJ3AeA2W1sHq_1J993C9Tn4AVKaP7w</recordid><startdate>202305</startdate><enddate>202305</enddate><creator>Inoue, Yoshihiro</creator><creator>Phuong Vy, Trinh Thi</creator><creator>Singkaravanit‐Ogawa, Suthitar</creator><creator>Zhang, Ru</creator><creator>Yamada, Kohji</creator><creator>Ogawa, Taiki</creator><creator>Ishizuka, Junya</creator><creator>Narusaka, Yoshihiro</creator><creator>Takano, Yoshitaka</creator><general>Wiley Subscription Services, 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><orcidid>https://orcid.org/0000-0002-0353-1726</orcidid><orcidid>https://orcid.org/0000-0003-1427-1322</orcidid></search><sort><creationdate>202305</creationdate><title>Selective deployment of virulence effectors correlates with host specificity in a fungal plant pathogen</title><author>Inoue, Yoshihiro ; Phuong Vy, Trinh Thi ; Singkaravanit‐Ogawa, Suthitar ; Zhang, Ru ; Yamada, Kohji ; Ogawa, Taiki ; Ishizuka, Junya ; Narusaka, Yoshihiro ; Takano, Yoshitaka</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4980-987f0b69c59f2a277e4a95b0fe863775ed243b9a892fae75527eb7bcfc41f06f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Colletotrichum orbiculare</topic><topic>Cucumis sativus - microbiology</topic><topic>Cucurbitaceae - genetics</topic><topic>Cucurbitaceae - metabolism</topic><topic>Cucurbitaceae - microbiology</topic><topic>Deployment</topic><topic>Effectors</topic><topic>Fungal Proteins - genetics</topic><topic>Fungal Proteins - metabolism</topic><topic>Fungi</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Host Specificity</topic><topic>Hosts</topic><topic>Nicotiana - genetics</topic><topic>Nicotiana benthamiana</topic><topic>Pathogens</topic><topic>Phylogeny</topic><topic>phytopathogenic fungi</topic><topic>Plant Diseases - microbiology</topic><topic>Proteins</topic><topic>Secretion</topic><topic>Solanaceae</topic><topic>Specificity</topic><topic>Tobacco</topic><topic>transcriptional control</topic><topic>Transcriptome</topic><topic>Virulence</topic><topic>Virulence - genetics</topic><topic>virulence effector</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Inoue, Yoshihiro</creatorcontrib><creatorcontrib>Phuong Vy, Trinh Thi</creatorcontrib><creatorcontrib>Singkaravanit‐Ogawa, Suthitar</creatorcontrib><creatorcontrib>Zhang, Ru</creatorcontrib><creatorcontrib>Yamada, Kohji</creatorcontrib><creatorcontrib>Ogawa, Taiki</creatorcontrib><creatorcontrib>Ishizuka, Junya</creatorcontrib><creatorcontrib>Narusaka, Yoshihiro</creatorcontrib><creatorcontrib>Takano, Yoshitaka</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><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Inoue, Yoshihiro</au><au>Phuong Vy, Trinh Thi</au><au>Singkaravanit‐Ogawa, Suthitar</au><au>Zhang, Ru</au><au>Yamada, Kohji</au><au>Ogawa, Taiki</au><au>Ishizuka, Junya</au><au>Narusaka, Yoshihiro</au><au>Takano, Yoshitaka</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Selective deployment of virulence effectors correlates with host specificity in a fungal plant pathogen</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2023-05</date><risdate>2023</risdate><volume>238</volume><issue>4</issue><spage>1578</spage><epage>1592</epage><pages>1578-1592</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>Summary
The hemibiotrophic fungal plant pathogen Colletotrichum orbiculare is predicted to secrete hundreds of effector proteins when the pathogen infects cucurbit crops, such as cucumber and melon, and tobacco (Nicotiana benthamiana), a distantly related Solanaceae species. Here, we report the identification of sets of C. orbiculare effector genes that are differentially required for fungal virulence to two phylogenetically distant host species.
Through targeted gene knockout screening of C. orbiculare ‘core’ effector candidates defined based on in planta gene expression, we identified: four host‐specific virulence effectors (named effector proteins for cucurbit infection, or EPCs) that are required for full virulence of C. orbiculare to cucurbit hosts, but not to the Solanaceae host N. benthamiana; and five host‐nonspecific virulence effectors, which collectively contribute to fungal virulence to both hosts.
During host infection, only a small subset of genes, including the host‐specific EPC effector genes, showed preferential expression on one of the hosts, while gene expression profiles of the majority of other genes, including the five host‐nonspecific effector genes, were common to both hosts.
This work suggests that C. orbiculare adopts a host‐specific effector deployment strategy, in addition to general host‐blind virulence mechanisms, for adaptation to cucurbit hosts.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>36939621</pmid><doi>10.1111/nph.18790</doi><tpages>1592</tpages><orcidid>https://orcid.org/0000-0002-0353-1726</orcidid><orcidid>https://orcid.org/0000-0003-1427-1322</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Colletotrichum orbiculare Cucumis sativus - microbiology Cucurbitaceae - genetics Cucurbitaceae - metabolism Cucurbitaceae - microbiology Deployment Effectors Fungal Proteins - genetics Fungal Proteins - metabolism Fungi Gene expression Genes Host Specificity Hosts Nicotiana - genetics Nicotiana benthamiana Pathogens Phylogeny phytopathogenic fungi Plant Diseases - microbiology Proteins Secretion Solanaceae Specificity Tobacco transcriptional control Transcriptome Virulence Virulence - genetics virulence effector |
| title | Selective deployment of virulence effectors correlates with host specificity in a fungal plant pathogen |
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