Heat-induced SUMOylation differentially affects bacterial effectors in plant cells
Bacterial pathogens deliver effectors into host cells to suppress immunity. How host cells target these effectors is critical in pathogen-host interactions. SUMOylation, an important type of posttranslational modification in eukaryotic cells, plays a critical role in immunity, but its effect on bact...
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description | Bacterial pathogens deliver effectors into host cells to suppress immunity. How host cells target these effectors is critical in pathogen-host interactions. SUMOylation, an important type of posttranslational modification in eukaryotic cells, plays a critical role in immunity, but its effect on bacterial effectors remains unclear in plant cells. In this study, using bioinformatic and biochemical approaches, we found that at least 16 effectors from the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 are SUMOylated by the enzyme cascade from Arabidopsis thaliana. Mutation of SUMOylation sites on the effector HopB1 enhances its function in the induction of plant cell death via stability attenuation of a plant receptor kinase BRASSINOSTEROID INSENSITIVE 1 (BRI1)-ASSOCIATED RECEPTOR KINASE 1. By contrast, SUMOylation is essential for the function of another effector, HopG1, in the inhibition of mitochondria activity and jasmonic acid signaling. SUMOylation of both HopB1 and HopG1 is increased by heat treatment, and this modification modulates the functions of these 2 effectors in different ways in the regulation of plant survival rates, gene expression, and bacterial infection under high temperatures. Therefore, the current work on the SUMOylation of effectors in plant cells improves our understanding of the function of dynamic protein modifications in plant-pathogen interactions in response to environmental conditions. |
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How host cells target these effectors is critical in pathogen-host interactions. SUMOylation, an important type of posttranslational modification in eukaryotic cells, plays a critical role in immunity, but its effect on bacterial effectors remains unclear in plant cells. In this study, using bioinformatic and biochemical approaches, we found that at least 16 effectors from the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 are SUMOylated by the enzyme cascade from Arabidopsis thaliana. Mutation of SUMOylation sites on the effector HopB1 enhances its function in the induction of plant cell death via stability attenuation of a plant receptor kinase BRASSINOSTEROID INSENSITIVE 1 (BRI1)-ASSOCIATED RECEPTOR KINASE 1. By contrast, SUMOylation is essential for the function of another effector, HopG1, in the inhibition of mitochondria activity and jasmonic acid signaling. SUMOylation of both HopB1 and HopG1 is increased by heat treatment, and this modification modulates the functions of these 2 effectors in different ways in the regulation of plant survival rates, gene expression, and bacterial infection under high temperatures. Therefore, the current work on the SUMOylation of effectors in plant cells improves our understanding of the function of dynamic protein modifications in plant-pathogen interactions in response to environmental conditions.</description><identifier>ISSN: 1040-4651</identifier><identifier>ISSN: 1532-298X</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1093/plcell/koae049</identifier><identifier>PMID: 38445983</identifier><language>eng</language><publisher>England</publisher><subject>Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis - microbiology ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Cell Death ; Cyclopentanes - metabolism ; Gene Expression Regulation, Plant ; Host-Pathogen Interactions ; Hot Temperature ; Oxylipins - metabolism ; Plant Cells - metabolism ; Plant Cells - microbiology ; Plant Diseases - microbiology ; Pseudomonas syringae - pathogenicity ; Pseudomonas syringae - physiology ; Signal Transduction ; Sumoylation</subject><ispartof>The Plant cell, 2024-05, Vol.36 (6), p.2103-2116</ispartof><rights>The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c180t-9f98dfed4bf9d55e94236bb338c04a8f849db82792110d9d7899f06c5befa7053</cites><orcidid>0009-0005-3662-408X ; 0000-0001-9199-5346 ; 0000-0002-8262-9093 ; 0000-0002-2648-3181 ; 0000-0001-9177-5781 ; 0009-0001-3017-6918 ; 0000-0002-9828-371X ; 0009-0002-5593-5615 ; 0009-0003-1679-9152 ; 0009-0007-4208-2410 ; 0000-0002-9269-9052</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38445983$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Li, Wenliang</creatorcontrib><creatorcontrib>Liu, Wen</creatorcontrib><creatorcontrib>Xu, Zewei</creatorcontrib><creatorcontrib>Zhu, Chengluo</creatorcontrib><creatorcontrib>Han, Danlu</creatorcontrib><creatorcontrib>Liao, Jianwei</creatorcontrib><creatorcontrib>Li, Kun</creatorcontrib><creatorcontrib>Tang, Xiaoyan</creatorcontrib><creatorcontrib>Xie, Qi</creatorcontrib><creatorcontrib>Yang, Chengwei</creatorcontrib><creatorcontrib>Lai, Jianbin</creatorcontrib><title>Heat-induced SUMOylation differentially affects bacterial effectors in plant cells</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>Bacterial pathogens deliver effectors into host cells to suppress immunity. How host cells target these effectors is critical in pathogen-host interactions. SUMOylation, an important type of posttranslational modification in eukaryotic cells, plays a critical role in immunity, but its effect on bacterial effectors remains unclear in plant cells. In this study, using bioinformatic and biochemical approaches, we found that at least 16 effectors from the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 are SUMOylated by the enzyme cascade from Arabidopsis thaliana. Mutation of SUMOylation sites on the effector HopB1 enhances its function in the induction of plant cell death via stability attenuation of a plant receptor kinase BRASSINOSTEROID INSENSITIVE 1 (BRI1)-ASSOCIATED RECEPTOR KINASE 1. By contrast, SUMOylation is essential for the function of another effector, HopG1, in the inhibition of mitochondria activity and jasmonic acid signaling. SUMOylation of both HopB1 and HopG1 is increased by heat treatment, and this modification modulates the functions of these 2 effectors in different ways in the regulation of plant survival rates, gene expression, and bacterial infection under high temperatures. Therefore, the current work on the SUMOylation of effectors in plant cells improves our understanding of the function of dynamic protein modifications in plant-pathogen interactions in response to environmental conditions.</description><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - microbiology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Cell Death</subject><subject>Cyclopentanes - metabolism</subject><subject>Gene Expression Regulation, Plant</subject><subject>Host-Pathogen Interactions</subject><subject>Hot Temperature</subject><subject>Oxylipins - metabolism</subject><subject>Plant Cells - metabolism</subject><subject>Plant Cells - microbiology</subject><subject>Plant Diseases - microbiology</subject><subject>Pseudomonas syringae - pathogenicity</subject><subject>Pseudomonas syringae - physiology</subject><subject>Signal Transduction</subject><subject>Sumoylation</subject><issn>1040-4651</issn><issn>1532-298X</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNo9kL1PwzAQxS0EoqWwMiKPLGn9lcYeUUUpUlEloBJb5NhnKeAmwXaG_vektDDd3dO7p6cfQreUTClRfNZ5A97PvloNRKgzNKY5ZxlT8uN82IkgmZjndISuYvwkhNCCqks04lKIXEk-Rq8r0CmrG9sbsPht-7LZe53qtsG2dg4CNKnW3u-xHi6TIq60SRAGDcOv0oaI6wZ3XjcJH7rEa3ThtI9wc5oTtF0-vi9W2Xrz9Lx4WGeGSpIy5ZS0DqyonLJ5DkowPq8qzqUhQksnhbKVZIVilBKrbCGVcmRu8gqcLkjOJ-j-mNuF9ruHmMpdHQ8NdANtH0umuGSyYJIP1unRakIbYwBXdqHe6bAvKSkPHMsjx_LEcXi4O2X31Q7sv_0PHP8Bqxtxzw</recordid><startdate>20240529</startdate><enddate>20240529</enddate><creator>Li, Wenliang</creator><creator>Liu, Wen</creator><creator>Xu, Zewei</creator><creator>Zhu, Chengluo</creator><creator>Han, Danlu</creator><creator>Liao, Jianwei</creator><creator>Li, Kun</creator><creator>Tang, Xiaoyan</creator><creator>Xie, Qi</creator><creator>Yang, Chengwei</creator><creator>Lai, Jianbin</creator><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>7X8</scope><orcidid>https://orcid.org/0009-0005-3662-408X</orcidid><orcidid>https://orcid.org/0000-0001-9199-5346</orcidid><orcidid>https://orcid.org/0000-0002-8262-9093</orcidid><orcidid>https://orcid.org/0000-0002-2648-3181</orcidid><orcidid>https://orcid.org/0000-0001-9177-5781</orcidid><orcidid>https://orcid.org/0009-0001-3017-6918</orcidid><orcidid>https://orcid.org/0000-0002-9828-371X</orcidid><orcidid>https://orcid.org/0009-0002-5593-5615</orcidid><orcidid>https://orcid.org/0009-0003-1679-9152</orcidid><orcidid>https://orcid.org/0009-0007-4208-2410</orcidid><orcidid>https://orcid.org/0000-0002-9269-9052</orcidid></search><sort><creationdate>20240529</creationdate><title>Heat-induced SUMOylation differentially affects bacterial effectors in plant cells</title><author>Li, Wenliang ; Liu, Wen ; Xu, Zewei ; Zhu, Chengluo ; Han, Danlu ; Liao, Jianwei ; Li, Kun ; Tang, Xiaoyan ; Xie, Qi ; Yang, Chengwei ; Lai, Jianbin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c180t-9f98dfed4bf9d55e94236bb338c04a8f849db82792110d9d7899f06c5befa7053</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis - microbiology</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Cell Death</topic><topic>Cyclopentanes - metabolism</topic><topic>Gene Expression Regulation, Plant</topic><topic>Host-Pathogen Interactions</topic><topic>Hot Temperature</topic><topic>Oxylipins - metabolism</topic><topic>Plant Cells - metabolism</topic><topic>Plant Cells - microbiology</topic><topic>Plant Diseases - microbiology</topic><topic>Pseudomonas syringae - pathogenicity</topic><topic>Pseudomonas syringae - physiology</topic><topic>Signal Transduction</topic><topic>Sumoylation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Li, Wenliang</creatorcontrib><creatorcontrib>Liu, Wen</creatorcontrib><creatorcontrib>Xu, Zewei</creatorcontrib><creatorcontrib>Zhu, Chengluo</creatorcontrib><creatorcontrib>Han, Danlu</creatorcontrib><creatorcontrib>Liao, Jianwei</creatorcontrib><creatorcontrib>Li, Kun</creatorcontrib><creatorcontrib>Tang, Xiaoyan</creatorcontrib><creatorcontrib>Xie, Qi</creatorcontrib><creatorcontrib>Yang, Chengwei</creatorcontrib><creatorcontrib>Lai, Jianbin</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>The Plant cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Li, Wenliang</au><au>Liu, Wen</au><au>Xu, Zewei</au><au>Zhu, Chengluo</au><au>Han, Danlu</au><au>Liao, Jianwei</au><au>Li, Kun</au><au>Tang, Xiaoyan</au><au>Xie, Qi</au><au>Yang, Chengwei</au><au>Lai, Jianbin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Heat-induced SUMOylation differentially affects bacterial effectors in plant cells</atitle><jtitle>The Plant cell</jtitle><addtitle>Plant Cell</addtitle><date>2024-05-29</date><risdate>2024</risdate><volume>36</volume><issue>6</issue><spage>2103</spage><epage>2116</epage><pages>2103-2116</pages><issn>1040-4651</issn><issn>1532-298X</issn><eissn>1532-298X</eissn><abstract>Bacterial pathogens deliver effectors into host cells to suppress immunity. How host cells target these effectors is critical in pathogen-host interactions. SUMOylation, an important type of posttranslational modification in eukaryotic cells, plays a critical role in immunity, but its effect on bacterial effectors remains unclear in plant cells. In this study, using bioinformatic and biochemical approaches, we found that at least 16 effectors from the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 are SUMOylated by the enzyme cascade from Arabidopsis thaliana. Mutation of SUMOylation sites on the effector HopB1 enhances its function in the induction of plant cell death via stability attenuation of a plant receptor kinase BRASSINOSTEROID INSENSITIVE 1 (BRI1)-ASSOCIATED RECEPTOR KINASE 1. By contrast, SUMOylation is essential for the function of another effector, HopG1, in the inhibition of mitochondria activity and jasmonic acid signaling. SUMOylation of both HopB1 and HopG1 is increased by heat treatment, and this modification modulates the functions of these 2 effectors in different ways in the regulation of plant survival rates, gene expression, and bacterial infection under high temperatures. Therefore, the current work on the SUMOylation of effectors in plant cells improves our understanding of the function of dynamic protein modifications in plant-pathogen interactions in response to environmental conditions.</abstract><cop>England</cop><pmid>38445983</pmid><doi>10.1093/plcell/koae049</doi><tpages>14</tpages><orcidid>https://orcid.org/0009-0005-3662-408X</orcidid><orcidid>https://orcid.org/0000-0001-9199-5346</orcidid><orcidid>https://orcid.org/0000-0002-8262-9093</orcidid><orcidid>https://orcid.org/0000-0002-2648-3181</orcidid><orcidid>https://orcid.org/0000-0001-9177-5781</orcidid><orcidid>https://orcid.org/0009-0001-3017-6918</orcidid><orcidid>https://orcid.org/0000-0002-9828-371X</orcidid><orcidid>https://orcid.org/0009-0002-5593-5615</orcidid><orcidid>https://orcid.org/0009-0003-1679-9152</orcidid><orcidid>https://orcid.org/0009-0007-4208-2410</orcidid><orcidid>https://orcid.org/0000-0002-9269-9052</orcidid></addata></record> |
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subjects | Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis - microbiology Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Bacterial Proteins - genetics Bacterial Proteins - metabolism Cell Death Cyclopentanes - metabolism Gene Expression Regulation, Plant Host-Pathogen Interactions Hot Temperature Oxylipins - metabolism Plant Cells - metabolism Plant Cells - microbiology Plant Diseases - microbiology Pseudomonas syringae - pathogenicity Pseudomonas syringae - physiology Signal Transduction Sumoylation |
title | Heat-induced SUMOylation differentially affects bacterial effectors in plant cells |
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