Protein phosphatase StTOPP6 negatively regulates potato bacterial wilt resistance by modulating MAPK signaling
Knock down of StTOPP6enhances resistance to bacterial wilt in potato by activating the MAPK3-mediated pathway and inducing accumulation of reactive oxygen species. Abstract Potato (Solanum tuberosum) is an important crop globally and is grown across many regions in China, where it ranks fourth in th...
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creator | Wang, Bingsen Huang, Mengshu He, Wenfeng Wang, Yuqi Yu, Liu Zhou, Dan Meng, Chengzhen Cheng, Dong Qiu, Huishan Tan, Xiaodan Song, Botao Chen, Huilan |
description | Knock down of StTOPP6enhances resistance to bacterial wilt in potato by activating the MAPK3-mediated pathway and inducing accumulation of reactive oxygen species.
Abstract
Potato (Solanum tuberosum) is an important crop globally and is grown across many regions in China, where it ranks fourth in the list of staple foods. However, its production and quality are severely affected by bacterial wilt caused by Ralstonia solanacearum. In this study, we identified StTOPP6, which belongs to the type one protein phosphatase (TOPP) family, and found that transient knock down of StTOPP6 in potato increased resistance against R. solanacearum. RNA-seq analysis showed that knock down of StTOPP6 activated immune responses, and this defense activation partly depended on the mitogen-activated protein kinase (MAPK) signal pathway. StTOPP6 inhibited the expression of StMAPK3, while overexpression of StMAPK3 enhanced resistance to R. solanacearum, supporting the negative role of StTOPP6 in plant immunity. Consistent with the results of knock down of StTOPP6, overexpressing the phosphatase-dead mutation StTOPP6m also attenuated infection and up-regulated MAPK3, showing that StTOPP6 activity is required for disease. Furthermore, we found that StTOPP6 affected the StMAPK3-mediated downstream defense pathway, eventually suppressing the accumulation of reactive oxygen species (ROS). Consistent with these findings, plants with knock down of StTOPP6, overexpression of StTOPP6m, and overexpression of StMAPK3 all displayed ROS accumulation and enhanced resistance to R. solanacearum. Taken together, the findings of our study demonstrate that StTOPP6 negatively regulates resistance to bacterial wilt by affecting the MAPK3-mediated pathway. |
doi_str_mv | 10.1093/jxb/erad145 |
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Abstract
Potato (Solanum tuberosum) is an important crop globally and is grown across many regions in China, where it ranks fourth in the list of staple foods. However, its production and quality are severely affected by bacterial wilt caused by Ralstonia solanacearum. In this study, we identified StTOPP6, which belongs to the type one protein phosphatase (TOPP) family, and found that transient knock down of StTOPP6 in potato increased resistance against R. solanacearum. RNA-seq analysis showed that knock down of StTOPP6 activated immune responses, and this defense activation partly depended on the mitogen-activated protein kinase (MAPK) signal pathway. StTOPP6 inhibited the expression of StMAPK3, while overexpression of StMAPK3 enhanced resistance to R. solanacearum, supporting the negative role of StTOPP6 in plant immunity. Consistent with the results of knock down of StTOPP6, overexpressing the phosphatase-dead mutation StTOPP6m also attenuated infection and up-regulated MAPK3, showing that StTOPP6 activity is required for disease. Furthermore, we found that StTOPP6 affected the StMAPK3-mediated downstream defense pathway, eventually suppressing the accumulation of reactive oxygen species (ROS). Consistent with these findings, plants with knock down of StTOPP6, overexpression of StTOPP6m, and overexpression of StMAPK3 all displayed ROS accumulation and enhanced resistance to R. solanacearum. Taken together, the findings of our study demonstrate that StTOPP6 negatively regulates resistance to bacterial wilt by affecting the MAPK3-mediated pathway.</description><identifier>ISSN: 0022-0957</identifier><identifier>EISSN: 1460-2431</identifier><identifier>DOI: 10.1093/jxb/erad145</identifier><identifier>PMID: 37086267</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Disease Resistance - genetics ; Mitogen-Activated Protein Kinases - genetics ; Mitogen-Activated Protein Kinases - metabolism ; Phosphoprotein Phosphatases - metabolism ; Plant Diseases - microbiology ; Ralstonia solanacearum - physiology ; Reactive Oxygen Species - metabolism ; Signal Transduction ; Solanum tuberosum - metabolism</subject><ispartof>Journal of experimental botany, 2023-08, Vol.74 (14), p.4208-4224</ispartof><rights>The Author(s) 2023. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com 2023</rights><rights>The Author(s) 2023. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c320t-55915646021486386af2ab02821647045a976249ba42254a6dd769977896a2f83</citedby><cites>FETCH-LOGICAL-c320t-55915646021486386af2ab02821647045a976249ba42254a6dd769977896a2f83</cites><orcidid>0000-0002-6626-7897 ; 0000-0001-5704-7051 ; 0000-0002-8493-1181</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37086267$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Bingsen</creatorcontrib><creatorcontrib>Huang, Mengshu</creatorcontrib><creatorcontrib>He, Wenfeng</creatorcontrib><creatorcontrib>Wang, Yuqi</creatorcontrib><creatorcontrib>Yu, Liu</creatorcontrib><creatorcontrib>Zhou, Dan</creatorcontrib><creatorcontrib>Meng, Chengzhen</creatorcontrib><creatorcontrib>Cheng, Dong</creatorcontrib><creatorcontrib>Qiu, Huishan</creatorcontrib><creatorcontrib>Tan, Xiaodan</creatorcontrib><creatorcontrib>Song, Botao</creatorcontrib><creatorcontrib>Chen, Huilan</creatorcontrib><title>Protein phosphatase StTOPP6 negatively regulates potato bacterial wilt resistance by modulating MAPK signaling</title><title>Journal of experimental botany</title><addtitle>J Exp Bot</addtitle><description>Knock down of StTOPP6enhances resistance to bacterial wilt in potato by activating the MAPK3-mediated pathway and inducing accumulation of reactive oxygen species.
Abstract
Potato (Solanum tuberosum) is an important crop globally and is grown across many regions in China, where it ranks fourth in the list of staple foods. However, its production and quality are severely affected by bacterial wilt caused by Ralstonia solanacearum. In this study, we identified StTOPP6, which belongs to the type one protein phosphatase (TOPP) family, and found that transient knock down of StTOPP6 in potato increased resistance against R. solanacearum. RNA-seq analysis showed that knock down of StTOPP6 activated immune responses, and this defense activation partly depended on the mitogen-activated protein kinase (MAPK) signal pathway. StTOPP6 inhibited the expression of StMAPK3, while overexpression of StMAPK3 enhanced resistance to R. solanacearum, supporting the negative role of StTOPP6 in plant immunity. Consistent with the results of knock down of StTOPP6, overexpressing the phosphatase-dead mutation StTOPP6m also attenuated infection and up-regulated MAPK3, showing that StTOPP6 activity is required for disease. Furthermore, we found that StTOPP6 affected the StMAPK3-mediated downstream defense pathway, eventually suppressing the accumulation of reactive oxygen species (ROS). Consistent with these findings, plants with knock down of StTOPP6, overexpression of StTOPP6m, and overexpression of StMAPK3 all displayed ROS accumulation and enhanced resistance to R. solanacearum. Taken together, the findings of our study demonstrate that StTOPP6 negatively regulates resistance to bacterial wilt by affecting the MAPK3-mediated pathway.</description><subject>Disease Resistance - genetics</subject><subject>Mitogen-Activated Protein Kinases - genetics</subject><subject>Mitogen-Activated Protein Kinases - metabolism</subject><subject>Phosphoprotein Phosphatases - metabolism</subject><subject>Plant Diseases - microbiology</subject><subject>Ralstonia solanacearum - physiology</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Signal Transduction</subject><subject>Solanum tuberosum - metabolism</subject><issn>0022-0957</issn><issn>1460-2431</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kM9LwzAUgIMobk5P3iUnEaQuSZO0PY7hL5xs4DyX1zbbMrqmJqm6_96MTY-eHo_38cH7ELqk5I6SLB6uv4uhslBRLo5Qn3JJIsZjeoz6hDAWkUwkPXTm3JoQIogQp6gXJySVTCZ91Mys8Uo3uF0Z167Ag1P4zc-ns5nEjVqC15-q3mKrll0NXjncGg_e4AJKr6yGGn_p2oe7085DUypcbPHGVDtaN0v8Opq9YKeXDdRhPUcnC6idujjMAXp_uJ-Pn6LJ9PF5PJpEZcyIj4TIqJDhE0Z5KuNUwoJBQVjKqOQJ4QKyRDKeFcAZExxkVSUyy5IkzSSwRRoP0M3e21rz0Snn8412papraJTpXM7SkIKlQRbQ2z1aWuOcVYu8tXoDdptTku8C5yFwfggc6KuDuCs2qvpjf4sG4HoPmK791_QDp_2EGw</recordid><startdate>20230803</startdate><enddate>20230803</enddate><creator>Wang, Bingsen</creator><creator>Huang, Mengshu</creator><creator>He, Wenfeng</creator><creator>Wang, Yuqi</creator><creator>Yu, Liu</creator><creator>Zhou, Dan</creator><creator>Meng, Chengzhen</creator><creator>Cheng, Dong</creator><creator>Qiu, Huishan</creator><creator>Tan, Xiaodan</creator><creator>Song, Botao</creator><creator>Chen, Huilan</creator><general>Oxford University Press</general><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/0000-0002-6626-7897</orcidid><orcidid>https://orcid.org/0000-0001-5704-7051</orcidid><orcidid>https://orcid.org/0000-0002-8493-1181</orcidid></search><sort><creationdate>20230803</creationdate><title>Protein phosphatase StTOPP6 negatively regulates potato bacterial wilt resistance by modulating MAPK signaling</title><author>Wang, Bingsen ; Huang, Mengshu ; He, Wenfeng ; Wang, Yuqi ; Yu, Liu ; Zhou, Dan ; Meng, Chengzhen ; Cheng, Dong ; Qiu, Huishan ; Tan, Xiaodan ; Song, Botao ; Chen, Huilan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c320t-55915646021486386af2ab02821647045a976249ba42254a6dd769977896a2f83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Disease Resistance - genetics</topic><topic>Mitogen-Activated Protein Kinases - genetics</topic><topic>Mitogen-Activated Protein Kinases - metabolism</topic><topic>Phosphoprotein Phosphatases - metabolism</topic><topic>Plant Diseases - microbiology</topic><topic>Ralstonia solanacearum - physiology</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>Signal Transduction</topic><topic>Solanum tuberosum - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Bingsen</creatorcontrib><creatorcontrib>Huang, Mengshu</creatorcontrib><creatorcontrib>He, Wenfeng</creatorcontrib><creatorcontrib>Wang, Yuqi</creatorcontrib><creatorcontrib>Yu, Liu</creatorcontrib><creatorcontrib>Zhou, Dan</creatorcontrib><creatorcontrib>Meng, Chengzhen</creatorcontrib><creatorcontrib>Cheng, Dong</creatorcontrib><creatorcontrib>Qiu, Huishan</creatorcontrib><creatorcontrib>Tan, Xiaodan</creatorcontrib><creatorcontrib>Song, Botao</creatorcontrib><creatorcontrib>Chen, Huilan</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>Journal of experimental botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Bingsen</au><au>Huang, Mengshu</au><au>He, Wenfeng</au><au>Wang, Yuqi</au><au>Yu, Liu</au><au>Zhou, Dan</au><au>Meng, Chengzhen</au><au>Cheng, Dong</au><au>Qiu, Huishan</au><au>Tan, Xiaodan</au><au>Song, Botao</au><au>Chen, Huilan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Protein phosphatase StTOPP6 negatively regulates potato bacterial wilt resistance by modulating MAPK signaling</atitle><jtitle>Journal of experimental botany</jtitle><addtitle>J Exp Bot</addtitle><date>2023-08-03</date><risdate>2023</risdate><volume>74</volume><issue>14</issue><spage>4208</spage><epage>4224</epage><pages>4208-4224</pages><issn>0022-0957</issn><eissn>1460-2431</eissn><abstract>Knock down of StTOPP6enhances resistance to bacterial wilt in potato by activating the MAPK3-mediated pathway and inducing accumulation of reactive oxygen species.
Abstract
Potato (Solanum tuberosum) is an important crop globally and is grown across many regions in China, where it ranks fourth in the list of staple foods. However, its production and quality are severely affected by bacterial wilt caused by Ralstonia solanacearum. In this study, we identified StTOPP6, which belongs to the type one protein phosphatase (TOPP) family, and found that transient knock down of StTOPP6 in potato increased resistance against R. solanacearum. RNA-seq analysis showed that knock down of StTOPP6 activated immune responses, and this defense activation partly depended on the mitogen-activated protein kinase (MAPK) signal pathway. StTOPP6 inhibited the expression of StMAPK3, while overexpression of StMAPK3 enhanced resistance to R. solanacearum, supporting the negative role of StTOPP6 in plant immunity. Consistent with the results of knock down of StTOPP6, overexpressing the phosphatase-dead mutation StTOPP6m also attenuated infection and up-regulated MAPK3, showing that StTOPP6 activity is required for disease. Furthermore, we found that StTOPP6 affected the StMAPK3-mediated downstream defense pathway, eventually suppressing the accumulation of reactive oxygen species (ROS). Consistent with these findings, plants with knock down of StTOPP6, overexpression of StTOPP6m, and overexpression of StMAPK3 all displayed ROS accumulation and enhanced resistance to R. solanacearum. Taken together, the findings of our study demonstrate that StTOPP6 negatively regulates resistance to bacterial wilt by affecting the MAPK3-mediated pathway.</abstract><cop>UK</cop><pub>Oxford University Press</pub><pmid>37086267</pmid><doi>10.1093/jxb/erad145</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-6626-7897</orcidid><orcidid>https://orcid.org/0000-0001-5704-7051</orcidid><orcidid>https://orcid.org/0000-0002-8493-1181</orcidid></addata></record> |
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subjects | Disease Resistance - genetics Mitogen-Activated Protein Kinases - genetics Mitogen-Activated Protein Kinases - metabolism Phosphoprotein Phosphatases - metabolism Plant Diseases - microbiology Ralstonia solanacearum - physiology Reactive Oxygen Species - metabolism Signal Transduction Solanum tuberosum - metabolism |
title | Protein phosphatase StTOPP6 negatively regulates potato bacterial wilt resistance by modulating MAPK signaling |
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