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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Veröffentlicht in:Journal of experimental botany 2023-08, Vol.74 (14), p.4208-4224
Hauptverfasser: Wang, Bingsen, Huang, Mengshu, He, Wenfeng, Wang, Yuqi, Yu, Liu, Zhou, Dan, Meng, Chengzhen, Cheng, Dong, Qiu, Huishan, Tan, Xiaodan, Song, Botao, Chen, Huilan
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container_issue 14
container_start_page 4208
container_title Journal of experimental botany
container_volume 74
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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source Oxford University Press Journals All Titles (1996-Current); MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection
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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