GmMKK4‐activated GmMPK6 stimulates GmERF113 to trigger resistance to Phytophthora sojae in soybean
SUMMARY Phytophthora root and stem rot is a worldwide soybean (Glycine max) disease caused by the soil‐borne pathogen Phytophthora sojae. This disease is devastating to soybean production, so improvement of resistance to P. sojae is a major target in soybean breeding. Mitogen‐activated protein kinas...
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Veröffentlicht in: | The Plant journal : for cell and molecular biology 2022-07, Vol.111 (2), p.473-495 |
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creator | Gao, Hong Jiang, Liangyu Du, Banghan Ning, Bin Ding, Xiaodong Zhang, Chuanzhong Song, Bo Liu, Shanshan Zhao, Ming Zhao, Yuxin Rong, Tianyu Liu, Dongxue Wu, Junjiang Xu, Pengfei Zhang, Shuzhen |
description | SUMMARY
Phytophthora root and stem rot is a worldwide soybean (Glycine max) disease caused by the soil‐borne pathogen Phytophthora sojae. This disease is devastating to soybean production, so improvement of resistance to P. sojae is a major target in soybean breeding. Mitogen‐activated protein kinase (MAPK) cascades are important signaling modules that convert environmental stimuli into cellular responses. Compared with extensive studies in Arabidopsis, the molecular mechanism of MAPK cascades in soybean disease resistance is barely elucidated. In this work, we found that the gene expression of mitogen‐activated protein kinase 6 (GmMPK6) was potently induced by P. sojae infection in the disease‐resistant soybean cultivar ‘Suinong 10’. Overexpression of GmMPK6 in soybean resulted in enhanced resistance to P. sojae and silencing of GmMPK6 led to the opposite phenotype. In our attempt to dissect the role of GmMPK6 in soybean resistance to phytophthora disease, we found that MAPK kinase 4 (GmMKK4) and the ERF transcription factor GmERF113 physically interact with GmMPK6, and we determined that GmMKK4 could phosphorylate and activate GmMPK6, which could subsequently phosphorylate GmERF113 upon P. sojae infection, suggesting that P. sojae can stimulate the GmMKK4–GmMPK6–GmERF113 signaling pathway in soybean. Moreover, phosphorylation of GmERF113 by the GmMKK4–GmMPK6 module promoted GmERF113 stability, nuclear localization and transcriptional activity, which significantly enhanced expression of the defense‐related genes GmPR1 and GmPR10‐1 and hence improved disease resistance of the transgenic soybean seedlings. In all, our data reveal that the GmMKK4–GmMPK6–GmERF113 cascade triggers resistance to P. sojae in soybean and shed light on functions of MAPK kinases in plant disease resistance.
Significance Statement
The GmMKK4–GmMPK6–GmERF113 cascade enhances resistance to soybean (Glycine max) phytophthora disease by successive phosphorylation events triggered by Phytophthora sojae. Our work provides new perspectives to develop strategies to improve plant disease resistance and insights into the roles of MAPK cascades in resistance against root and stem rot diseases. |
doi_str_mv | 10.1111/tpj.15809 |
format | Article |
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Phytophthora root and stem rot is a worldwide soybean (Glycine max) disease caused by the soil‐borne pathogen Phytophthora sojae. This disease is devastating to soybean production, so improvement of resistance to P. sojae is a major target in soybean breeding. Mitogen‐activated protein kinase (MAPK) cascades are important signaling modules that convert environmental stimuli into cellular responses. Compared with extensive studies in Arabidopsis, the molecular mechanism of MAPK cascades in soybean disease resistance is barely elucidated. In this work, we found that the gene expression of mitogen‐activated protein kinase 6 (GmMPK6) was potently induced by P. sojae infection in the disease‐resistant soybean cultivar ‘Suinong 10’. Overexpression of GmMPK6 in soybean resulted in enhanced resistance to P. sojae and silencing of GmMPK6 led to the opposite phenotype. In our attempt to dissect the role of GmMPK6 in soybean resistance to phytophthora disease, we found that MAPK kinase 4 (GmMKK4) and the ERF transcription factor GmERF113 physically interact with GmMPK6, and we determined that GmMKK4 could phosphorylate and activate GmMPK6, which could subsequently phosphorylate GmERF113 upon P. sojae infection, suggesting that P. sojae can stimulate the GmMKK4–GmMPK6–GmERF113 signaling pathway in soybean. Moreover, phosphorylation of GmERF113 by the GmMKK4–GmMPK6 module promoted GmERF113 stability, nuclear localization and transcriptional activity, which significantly enhanced expression of the defense‐related genes GmPR1 and GmPR10‐1 and hence improved disease resistance of the transgenic soybean seedlings. In all, our data reveal that the GmMKK4–GmMPK6–GmERF113 cascade triggers resistance to P. sojae in soybean and shed light on functions of MAPK kinases in plant disease resistance.
Significance Statement
The GmMKK4–GmMPK6–GmERF113 cascade enhances resistance to soybean (Glycine max) phytophthora disease by successive phosphorylation events triggered by Phytophthora sojae. Our work provides new perspectives to develop strategies to improve plant disease resistance and insights into the roles of MAPK cascades in resistance against root and stem rot diseases.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.15809</identifier><identifier>PMID: 35562858</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Arabidopsis - metabolism ; Crop production ; Cultivars ; Disease resistance ; Disease Resistance - genetics ; Environmental effects ; Ethylene response factor (ERF) transcription factor ; Gene expression ; Glycine max ; Glycine max - metabolism ; Kinases ; Localization ; MAP kinase ; Mitogen‐activated protein kinase cascade (MAPK) ; Modules ; Phenotypes ; Phosphorylation ; Phytophthora - physiology ; Phytophthora sojae ; Plant Breeding ; Plant diseases ; Plant immunity ; Plant Proteins - metabolism ; Protein kinase ; Proteins ; Seedlings ; Signal transduction ; Signaling ; soybean ; Soybeans ; Stem rot</subject><ispartof>The Plant journal : for cell and molecular biology, 2022-07, Vol.111 (2), p.473-495</ispartof><rights>2022 Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>Copyright © 2022 John Wiley & Sons Ltd and the Society for Experimental Biology</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3539-ea98dff609be8ba73085b13502ed526f518e25522256b51f551c9aa0b9794c8c3</citedby><cites>FETCH-LOGICAL-c3539-ea98dff609be8ba73085b13502ed526f518e25522256b51f551c9aa0b9794c8c3</cites><orcidid>0000-0003-3554-5855 ; 0000-0002-3311-0092</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%2Ftpj.15809$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.15809$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35562858$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gao, Hong</creatorcontrib><creatorcontrib>Jiang, Liangyu</creatorcontrib><creatorcontrib>Du, Banghan</creatorcontrib><creatorcontrib>Ning, Bin</creatorcontrib><creatorcontrib>Ding, Xiaodong</creatorcontrib><creatorcontrib>Zhang, Chuanzhong</creatorcontrib><creatorcontrib>Song, Bo</creatorcontrib><creatorcontrib>Liu, Shanshan</creatorcontrib><creatorcontrib>Zhao, Ming</creatorcontrib><creatorcontrib>Zhao, Yuxin</creatorcontrib><creatorcontrib>Rong, Tianyu</creatorcontrib><creatorcontrib>Liu, Dongxue</creatorcontrib><creatorcontrib>Wu, Junjiang</creatorcontrib><creatorcontrib>Xu, Pengfei</creatorcontrib><creatorcontrib>Zhang, Shuzhen</creatorcontrib><title>GmMKK4‐activated GmMPK6 stimulates GmERF113 to trigger resistance to Phytophthora sojae in soybean</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>SUMMARY
Phytophthora root and stem rot is a worldwide soybean (Glycine max) disease caused by the soil‐borne pathogen Phytophthora sojae. This disease is devastating to soybean production, so improvement of resistance to P. sojae is a major target in soybean breeding. Mitogen‐activated protein kinase (MAPK) cascades are important signaling modules that convert environmental stimuli into cellular responses. Compared with extensive studies in Arabidopsis, the molecular mechanism of MAPK cascades in soybean disease resistance is barely elucidated. In this work, we found that the gene expression of mitogen‐activated protein kinase 6 (GmMPK6) was potently induced by P. sojae infection in the disease‐resistant soybean cultivar ‘Suinong 10’. Overexpression of GmMPK6 in soybean resulted in enhanced resistance to P. sojae and silencing of GmMPK6 led to the opposite phenotype. In our attempt to dissect the role of GmMPK6 in soybean resistance to phytophthora disease, we found that MAPK kinase 4 (GmMKK4) and the ERF transcription factor GmERF113 physically interact with GmMPK6, and we determined that GmMKK4 could phosphorylate and activate GmMPK6, which could subsequently phosphorylate GmERF113 upon P. sojae infection, suggesting that P. sojae can stimulate the GmMKK4–GmMPK6–GmERF113 signaling pathway in soybean. Moreover, phosphorylation of GmERF113 by the GmMKK4–GmMPK6 module promoted GmERF113 stability, nuclear localization and transcriptional activity, which significantly enhanced expression of the defense‐related genes GmPR1 and GmPR10‐1 and hence improved disease resistance of the transgenic soybean seedlings. In all, our data reveal that the GmMKK4–GmMPK6–GmERF113 cascade triggers resistance to P. sojae in soybean and shed light on functions of MAPK kinases in plant disease resistance.
Significance Statement
The GmMKK4–GmMPK6–GmERF113 cascade enhances resistance to soybean (Glycine max) phytophthora disease by successive phosphorylation events triggered by Phytophthora sojae. Our work provides new perspectives to develop strategies to improve plant disease resistance and insights into the roles of MAPK cascades in resistance against root and stem rot diseases.</description><subject>Arabidopsis - metabolism</subject><subject>Crop production</subject><subject>Cultivars</subject><subject>Disease resistance</subject><subject>Disease Resistance - genetics</subject><subject>Environmental effects</subject><subject>Ethylene response factor (ERF) transcription factor</subject><subject>Gene expression</subject><subject>Glycine max</subject><subject>Glycine max - metabolism</subject><subject>Kinases</subject><subject>Localization</subject><subject>MAP kinase</subject><subject>Mitogen‐activated protein kinase cascade (MAPK)</subject><subject>Modules</subject><subject>Phenotypes</subject><subject>Phosphorylation</subject><subject>Phytophthora - physiology</subject><subject>Phytophthora sojae</subject><subject>Plant Breeding</subject><subject>Plant diseases</subject><subject>Plant immunity</subject><subject>Plant Proteins - metabolism</subject><subject>Protein kinase</subject><subject>Proteins</subject><subject>Seedlings</subject><subject>Signal transduction</subject><subject>Signaling</subject><subject>soybean</subject><subject>Soybeans</subject><subject>Stem rot</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kE1P3DAQhq2qqGxpD_yBKlIv7SHgsTOOfawQH-2CukIg9RY5yYTNKh-L7bTaW38Cv5FfgmEph0rMZUavHr0aPYztAz-AOIdhvToA1Ny8YTOQClMJ8tdbNuNG8TTPQOyy996vOIdcquwd25WISmjUM1af9hfzeXb_985Wof1tA9VJjBZzlfjQ9lMXEx-T48sTAJmEMQmuvbkhlzjyrQ92qOgxXSw3YVwvw3J0NvHjylLSDvHYlGSHD2ynsZ2nj897j12fHF8dnaXnP0-_H307TyuJ0qRkja6bRnFTki5tLrnGEiRyQTUK1SBoEohCCFQlQoMIlbGWlyY3WaUruce-bHvXbrydyIeib31FXWcHGidfCKUyzaMQiOjn_9DVOLkhfhcpAxowyzFSX7dU5UbvHTXF2rW9dZsCePGovojqiyf1kf303DiVPdUv5D_XETjcAn_ajjavNxVXix_bygezgoy1</recordid><startdate>202207</startdate><enddate>202207</enddate><creator>Gao, Hong</creator><creator>Jiang, Liangyu</creator><creator>Du, Banghan</creator><creator>Ning, Bin</creator><creator>Ding, Xiaodong</creator><creator>Zhang, Chuanzhong</creator><creator>Song, Bo</creator><creator>Liu, Shanshan</creator><creator>Zhao, Ming</creator><creator>Zhao, Yuxin</creator><creator>Rong, Tianyu</creator><creator>Liu, Dongxue</creator><creator>Wu, Junjiang</creator><creator>Xu, Pengfei</creator><creator>Zhang, Shuzhen</creator><general>Blackwell Publishing Ltd</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>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-3554-5855</orcidid><orcidid>https://orcid.org/0000-0002-3311-0092</orcidid></search><sort><creationdate>202207</creationdate><title>GmMKK4‐activated GmMPK6 stimulates GmERF113 to trigger resistance to Phytophthora sojae in soybean</title><author>Gao, Hong ; Jiang, Liangyu ; Du, Banghan ; Ning, Bin ; Ding, Xiaodong ; Zhang, Chuanzhong ; Song, Bo ; Liu, Shanshan ; Zhao, Ming ; Zhao, Yuxin ; Rong, Tianyu ; Liu, Dongxue ; Wu, Junjiang ; Xu, Pengfei ; Zhang, Shuzhen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3539-ea98dff609be8ba73085b13502ed526f518e25522256b51f551c9aa0b9794c8c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Arabidopsis - metabolism</topic><topic>Crop production</topic><topic>Cultivars</topic><topic>Disease resistance</topic><topic>Disease Resistance - genetics</topic><topic>Environmental effects</topic><topic>Ethylene response factor (ERF) transcription factor</topic><topic>Gene expression</topic><topic>Glycine max</topic><topic>Glycine max - metabolism</topic><topic>Kinases</topic><topic>Localization</topic><topic>MAP kinase</topic><topic>Mitogen‐activated protein kinase cascade (MAPK)</topic><topic>Modules</topic><topic>Phenotypes</topic><topic>Phosphorylation</topic><topic>Phytophthora - physiology</topic><topic>Phytophthora sojae</topic><topic>Plant Breeding</topic><topic>Plant diseases</topic><topic>Plant immunity</topic><topic>Plant Proteins - metabolism</topic><topic>Protein kinase</topic><topic>Proteins</topic><topic>Seedlings</topic><topic>Signal transduction</topic><topic>Signaling</topic><topic>soybean</topic><topic>Soybeans</topic><topic>Stem rot</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gao, Hong</creatorcontrib><creatorcontrib>Jiang, Liangyu</creatorcontrib><creatorcontrib>Du, Banghan</creatorcontrib><creatorcontrib>Ning, Bin</creatorcontrib><creatorcontrib>Ding, Xiaodong</creatorcontrib><creatorcontrib>Zhang, Chuanzhong</creatorcontrib><creatorcontrib>Song, Bo</creatorcontrib><creatorcontrib>Liu, Shanshan</creatorcontrib><creatorcontrib>Zhao, Ming</creatorcontrib><creatorcontrib>Zhao, Yuxin</creatorcontrib><creatorcontrib>Rong, Tianyu</creatorcontrib><creatorcontrib>Liu, Dongxue</creatorcontrib><creatorcontrib>Wu, Junjiang</creatorcontrib><creatorcontrib>Xu, Pengfei</creatorcontrib><creatorcontrib>Zhang, Shuzhen</creatorcontrib><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>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</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 Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gao, Hong</au><au>Jiang, Liangyu</au><au>Du, Banghan</au><au>Ning, Bin</au><au>Ding, Xiaodong</au><au>Zhang, Chuanzhong</au><au>Song, Bo</au><au>Liu, Shanshan</au><au>Zhao, Ming</au><au>Zhao, Yuxin</au><au>Rong, Tianyu</au><au>Liu, Dongxue</au><au>Wu, Junjiang</au><au>Xu, Pengfei</au><au>Zhang, Shuzhen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>GmMKK4‐activated GmMPK6 stimulates GmERF113 to trigger resistance to Phytophthora sojae in soybean</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2022-07</date><risdate>2022</risdate><volume>111</volume><issue>2</issue><spage>473</spage><epage>495</epage><pages>473-495</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>SUMMARY
Phytophthora root and stem rot is a worldwide soybean (Glycine max) disease caused by the soil‐borne pathogen Phytophthora sojae. This disease is devastating to soybean production, so improvement of resistance to P. sojae is a major target in soybean breeding. Mitogen‐activated protein kinase (MAPK) cascades are important signaling modules that convert environmental stimuli into cellular responses. Compared with extensive studies in Arabidopsis, the molecular mechanism of MAPK cascades in soybean disease resistance is barely elucidated. In this work, we found that the gene expression of mitogen‐activated protein kinase 6 (GmMPK6) was potently induced by P. sojae infection in the disease‐resistant soybean cultivar ‘Suinong 10’. Overexpression of GmMPK6 in soybean resulted in enhanced resistance to P. sojae and silencing of GmMPK6 led to the opposite phenotype. In our attempt to dissect the role of GmMPK6 in soybean resistance to phytophthora disease, we found that MAPK kinase 4 (GmMKK4) and the ERF transcription factor GmERF113 physically interact with GmMPK6, and we determined that GmMKK4 could phosphorylate and activate GmMPK6, which could subsequently phosphorylate GmERF113 upon P. sojae infection, suggesting that P. sojae can stimulate the GmMKK4–GmMPK6–GmERF113 signaling pathway in soybean. Moreover, phosphorylation of GmERF113 by the GmMKK4–GmMPK6 module promoted GmERF113 stability, nuclear localization and transcriptional activity, which significantly enhanced expression of the defense‐related genes GmPR1 and GmPR10‐1 and hence improved disease resistance of the transgenic soybean seedlings. In all, our data reveal that the GmMKK4–GmMPK6–GmERF113 cascade triggers resistance to P. sojae in soybean and shed light on functions of MAPK kinases in plant disease resistance.
Significance Statement
The GmMKK4–GmMPK6–GmERF113 cascade enhances resistance to soybean (Glycine max) phytophthora disease by successive phosphorylation events triggered by Phytophthora sojae. Our work provides new perspectives to develop strategies to improve plant disease resistance and insights into the roles of MAPK cascades in resistance against root and stem rot diseases.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>35562858</pmid><doi>10.1111/tpj.15809</doi><tpages>495</tpages><orcidid>https://orcid.org/0000-0003-3554-5855</orcidid><orcidid>https://orcid.org/0000-0002-3311-0092</orcidid></addata></record> |
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subjects | Arabidopsis - metabolism Crop production Cultivars Disease resistance Disease Resistance - genetics Environmental effects Ethylene response factor (ERF) transcription factor Gene expression Glycine max Glycine max - metabolism Kinases Localization MAP kinase Mitogen‐activated protein kinase cascade (MAPK) Modules Phenotypes Phosphorylation Phytophthora - physiology Phytophthora sojae Plant Breeding Plant diseases Plant immunity Plant Proteins - metabolism Protein kinase Proteins Seedlings Signal transduction Signaling soybean Soybeans Stem rot |
title | GmMKK4‐activated GmMPK6 stimulates GmERF113 to trigger resistance to Phytophthora sojae in soybean |
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