RAV1 family members function as transcriptional regulators and play a positive role in plant disease resistance
SUMMARY Phytopathogens pose a severe threat to agriculture and strengthening the plant defense response is an important strategy for disease control. Here, we report that AtRAV1, an AP2 and B3 domain‐containing transcription factor, is required for basal plant defense in Arabidopsis thaliana. The at...
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Veröffentlicht in: | The Plant journal : for cell and molecular biology 2023-04, Vol.114 (1), p.39-54 |
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creator | Chandan, Ravindra Kumar Kumar, Rahul Swain, Durga Madhab Ghosh, Srayan Bhagat, Prakash Kumar Patel, Sunita Bagler, Ganesh Sinha, Alok Krishna Jha, Gopaljee |
description | SUMMARY
Phytopathogens pose a severe threat to agriculture and strengthening the plant defense response is an important strategy for disease control. Here, we report that AtRAV1, an AP2 and B3 domain‐containing transcription factor, is required for basal plant defense in Arabidopsis thaliana. The atrav1 mutant lines demonstrate hyper‐susceptibility against fungal pathogens (Rhizoctonia solani and Botrytis cinerea), whereas AtRAV1 overexpressing lines exhibit disease resistance against them. Enhanced expression of various defense genes and activation of mitogen‐activated protein kinases (AtMPK3 and AtMPK6) are observed in the R. solani infected overexpressing lines, but not in the atrav1 mutant plants. An in vitro phosphorylation assay suggests AtRAV1 to be a novel phosphorylation target of AtMPK3. Bimolecular fluorescence complementation and yeast two‐hybrid assays support physical interactions between AtRAV1 and AtMPK3. Overexpression of the native as well as phospho‐mimic but not the phospho‐defective variant of AtRAV1 imparts disease resistance in the atrav1 mutant A. thaliana lines. On the other hand, overexpression of AtRAV1 fails to impart disease resistance in the atmpk3 mutant. These analyses emphasize that AtMPK3‐mediated phosphorylation of AtRAV1 is important for the elaboration of the defense response in A. thaliana. Considering that RAV1 homologs are conserved in diverse plant species, we propose that they can be gainfully deployed to impart disease resistance in agriculturally important crop plants. Indeed, overexpression of SlRAV1 (a member of the RAV1 family) imparts disease tolerance against not only fungal (R. solani and B. cinerea), but also against bacterial (Ralstonia solanacearum) pathogens in tomato, whereas silencing of the gene enhances disease susceptibility.
Significance Statement
AtRAV1 functions as a transcriptional regulator of the defense response in Arabidopsis thaliana and, upon overexpression, it imparts disease resistance. We demonstrate that AtRAV1 transcriptionally regulates mitogen‐activated protein kinases, while AtMPK3 modulates the AtRAV1 function through post‐translational modification (phosphorylation). We provide evidence that SlRAV1 (a member of the RAV1 family) can be gainfully deployed to impart broad‐spectrum disease resistance in tomato. |
doi_str_mv | 10.1111/tpj.16114 |
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Phytopathogens pose a severe threat to agriculture and strengthening the plant defense response is an important strategy for disease control. Here, we report that AtRAV1, an AP2 and B3 domain‐containing transcription factor, is required for basal plant defense in Arabidopsis thaliana. The atrav1 mutant lines demonstrate hyper‐susceptibility against fungal pathogens (Rhizoctonia solani and Botrytis cinerea), whereas AtRAV1 overexpressing lines exhibit disease resistance against them. Enhanced expression of various defense genes and activation of mitogen‐activated protein kinases (AtMPK3 and AtMPK6) are observed in the R. solani infected overexpressing lines, but not in the atrav1 mutant plants. An in vitro phosphorylation assay suggests AtRAV1 to be a novel phosphorylation target of AtMPK3. Bimolecular fluorescence complementation and yeast two‐hybrid assays support physical interactions between AtRAV1 and AtMPK3. Overexpression of the native as well as phospho‐mimic but not the phospho‐defective variant of AtRAV1 imparts disease resistance in the atrav1 mutant A. thaliana lines. On the other hand, overexpression of AtRAV1 fails to impart disease resistance in the atmpk3 mutant. These analyses emphasize that AtMPK3‐mediated phosphorylation of AtRAV1 is important for the elaboration of the defense response in A. thaliana. Considering that RAV1 homologs are conserved in diverse plant species, we propose that they can be gainfully deployed to impart disease resistance in agriculturally important crop plants. Indeed, overexpression of SlRAV1 (a member of the RAV1 family) imparts disease tolerance against not only fungal (R. solani and B. cinerea), but also against bacterial (Ralstonia solanacearum) pathogens in tomato, whereas silencing of the gene enhances disease susceptibility.
Significance Statement
AtRAV1 functions as a transcriptional regulator of the defense response in Arabidopsis thaliana and, upon overexpression, it imparts disease resistance. We demonstrate that AtRAV1 transcriptionally regulates mitogen‐activated protein kinases, while AtMPK3 modulates the AtRAV1 function through post‐translational modification (phosphorylation). We provide evidence that SlRAV1 (a member of the RAV1 family) can be gainfully deployed to impart broad‐spectrum disease resistance in tomato.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.16114</identifier><identifier>PMID: 36703574</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; bacterial wilt disease ; Complementation ; Defense mechanisms ; Disease control ; Disease resistance ; Disease Resistance - genetics ; Disease tolerance ; DNA-Binding Proteins - genetics ; Fungi ; Gene expression ; Gene Expression Regulation, Plant ; Kinases ; Mitogen-Activated Protein Kinases - metabolism ; Mutants ; necrotrophs ; Pathogens ; Phosphorylation ; phytohormone ; Plant diseases ; Plant Diseases - genetics ; Plant Diseases - microbiology ; Plant immunity ; Plant species ; post‐translational modification ; sheath blight disease ; Tomatoes ; Transcription activation ; transcriptional regulation ; Yeasts</subject><ispartof>The Plant journal : for cell and molecular biology, 2023-04, Vol.114 (1), p.39-54</ispartof><rights>2023 Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>Copyright © 2023 Society for Experimental Biology and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3884-ab18fa69685624cbad49d16c2e57ff0f7daa4bac07ee79edb77524d008b671ae3</citedby><cites>FETCH-LOGICAL-c3884-ab18fa69685624cbad49d16c2e57ff0f7daa4bac07ee79edb77524d008b671ae3</cites><orcidid>0000-0003-0820-9936 ; 0000-0002-3965-3135</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.16114$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.16114$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36703574$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chandan, Ravindra Kumar</creatorcontrib><creatorcontrib>Kumar, Rahul</creatorcontrib><creatorcontrib>Swain, Durga Madhab</creatorcontrib><creatorcontrib>Ghosh, Srayan</creatorcontrib><creatorcontrib>Bhagat, Prakash Kumar</creatorcontrib><creatorcontrib>Patel, Sunita</creatorcontrib><creatorcontrib>Bagler, Ganesh</creatorcontrib><creatorcontrib>Sinha, Alok Krishna</creatorcontrib><creatorcontrib>Jha, Gopaljee</creatorcontrib><title>RAV1 family members function as transcriptional regulators and play a positive role in plant disease resistance</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>SUMMARY
Phytopathogens pose a severe threat to agriculture and strengthening the plant defense response is an important strategy for disease control. Here, we report that AtRAV1, an AP2 and B3 domain‐containing transcription factor, is required for basal plant defense in Arabidopsis thaliana. The atrav1 mutant lines demonstrate hyper‐susceptibility against fungal pathogens (Rhizoctonia solani and Botrytis cinerea), whereas AtRAV1 overexpressing lines exhibit disease resistance against them. Enhanced expression of various defense genes and activation of mitogen‐activated protein kinases (AtMPK3 and AtMPK6) are observed in the R. solani infected overexpressing lines, but not in the atrav1 mutant plants. An in vitro phosphorylation assay suggests AtRAV1 to be a novel phosphorylation target of AtMPK3. Bimolecular fluorescence complementation and yeast two‐hybrid assays support physical interactions between AtRAV1 and AtMPK3. Overexpression of the native as well as phospho‐mimic but not the phospho‐defective variant of AtRAV1 imparts disease resistance in the atrav1 mutant A. thaliana lines. On the other hand, overexpression of AtRAV1 fails to impart disease resistance in the atmpk3 mutant. These analyses emphasize that AtMPK3‐mediated phosphorylation of AtRAV1 is important for the elaboration of the defense response in A. thaliana. Considering that RAV1 homologs are conserved in diverse plant species, we propose that they can be gainfully deployed to impart disease resistance in agriculturally important crop plants. Indeed, overexpression of SlRAV1 (a member of the RAV1 family) imparts disease tolerance against not only fungal (R. solani and B. cinerea), but also against bacterial (Ralstonia solanacearum) pathogens in tomato, whereas silencing of the gene enhances disease susceptibility.
Significance Statement
AtRAV1 functions as a transcriptional regulator of the defense response in Arabidopsis thaliana and, upon overexpression, it imparts disease resistance. We demonstrate that AtRAV1 transcriptionally regulates mitogen‐activated protein kinases, while AtMPK3 modulates the AtRAV1 function through post‐translational modification (phosphorylation). We provide evidence that SlRAV1 (a member of the RAV1 family) can be gainfully deployed to impart broad‐spectrum disease resistance in tomato.</description><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>bacterial wilt disease</subject><subject>Complementation</subject><subject>Defense mechanisms</subject><subject>Disease control</subject><subject>Disease resistance</subject><subject>Disease Resistance - genetics</subject><subject>Disease tolerance</subject><subject>DNA-Binding Proteins - genetics</subject><subject>Fungi</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Kinases</subject><subject>Mitogen-Activated Protein Kinases - metabolism</subject><subject>Mutants</subject><subject>necrotrophs</subject><subject>Pathogens</subject><subject>Phosphorylation</subject><subject>phytohormone</subject><subject>Plant diseases</subject><subject>Plant Diseases - genetics</subject><subject>Plant Diseases - microbiology</subject><subject>Plant immunity</subject><subject>Plant species</subject><subject>post‐translational modification</subject><subject>sheath blight disease</subject><subject>Tomatoes</subject><subject>Transcription activation</subject><subject>transcriptional regulation</subject><subject>Yeasts</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp10cFq3DAQBmBRWpptmkNfIAh6SQ9ONJYs2cewJGlLoCGkITczlsdBi205kt2yb19tNs2hUF0EPx8_0gxjn0CcQjpn87Q5BQ2g3rAVSF1kEuTDW7YSlRaZUZAfsA8xboQAI7V6zw6kNkIWRq2Yvz2_B97h4PotH2hoKETeLaOdnR85Rj4HHKMNbtoF2PNAj0uPs08Mx5ZPPW458slHN7tfxIPvibtxl48zb10kjCml6OKMo6WP7F2HfaSjl_uQ_by8uFt_za5_XH1bn19nVpalyrCBskNd6bLQubINtqpqQducCtN1ojMtomrQCkNkKmobY4pctUKUjTaAJA_Zyb53Cv5poTjXg4uW-vQs8kusc2MEQCmqItHP_9CNX0L6605VUORGyzKpL3tlg48xUFdPwQ0YtjWIereFOm2hft5CsscvjUszUPsq_449gbM9-O162v6_qb67-b6v_AMRWZKz</recordid><startdate>202304</startdate><enddate>202304</enddate><creator>Chandan, Ravindra Kumar</creator><creator>Kumar, Rahul</creator><creator>Swain, Durga Madhab</creator><creator>Ghosh, Srayan</creator><creator>Bhagat, Prakash Kumar</creator><creator>Patel, Sunita</creator><creator>Bagler, Ganesh</creator><creator>Sinha, Alok Krishna</creator><creator>Jha, Gopaljee</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/0000-0003-0820-9936</orcidid><orcidid>https://orcid.org/0000-0002-3965-3135</orcidid></search><sort><creationdate>202304</creationdate><title>RAV1 family members function as transcriptional regulators and play a positive role in plant disease resistance</title><author>Chandan, Ravindra Kumar ; Kumar, Rahul ; Swain, Durga Madhab ; Ghosh, Srayan ; Bhagat, Prakash Kumar ; Patel, Sunita ; Bagler, Ganesh ; Sinha, Alok Krishna ; Jha, Gopaljee</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3884-ab18fa69685624cbad49d16c2e57ff0f7daa4bac07ee79edb77524d008b671ae3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>bacterial wilt disease</topic><topic>Complementation</topic><topic>Defense mechanisms</topic><topic>Disease control</topic><topic>Disease resistance</topic><topic>Disease Resistance - genetics</topic><topic>Disease tolerance</topic><topic>DNA-Binding Proteins - genetics</topic><topic>Fungi</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>Kinases</topic><topic>Mitogen-Activated Protein Kinases - metabolism</topic><topic>Mutants</topic><topic>necrotrophs</topic><topic>Pathogens</topic><topic>Phosphorylation</topic><topic>phytohormone</topic><topic>Plant diseases</topic><topic>Plant Diseases - genetics</topic><topic>Plant Diseases - microbiology</topic><topic>Plant immunity</topic><topic>Plant species</topic><topic>post‐translational modification</topic><topic>sheath blight disease</topic><topic>Tomatoes</topic><topic>Transcription activation</topic><topic>transcriptional regulation</topic><topic>Yeasts</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chandan, Ravindra Kumar</creatorcontrib><creatorcontrib>Kumar, Rahul</creatorcontrib><creatorcontrib>Swain, Durga Madhab</creatorcontrib><creatorcontrib>Ghosh, Srayan</creatorcontrib><creatorcontrib>Bhagat, Prakash Kumar</creatorcontrib><creatorcontrib>Patel, Sunita</creatorcontrib><creatorcontrib>Bagler, Ganesh</creatorcontrib><creatorcontrib>Sinha, Alok Krishna</creatorcontrib><creatorcontrib>Jha, Gopaljee</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>Chandan, Ravindra Kumar</au><au>Kumar, Rahul</au><au>Swain, Durga Madhab</au><au>Ghosh, Srayan</au><au>Bhagat, Prakash Kumar</au><au>Patel, Sunita</au><au>Bagler, Ganesh</au><au>Sinha, Alok Krishna</au><au>Jha, Gopaljee</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>RAV1 family members function as transcriptional regulators and play a positive role in plant disease resistance</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2023-04</date><risdate>2023</risdate><volume>114</volume><issue>1</issue><spage>39</spage><epage>54</epage><pages>39-54</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>SUMMARY
Phytopathogens pose a severe threat to agriculture and strengthening the plant defense response is an important strategy for disease control. Here, we report that AtRAV1, an AP2 and B3 domain‐containing transcription factor, is required for basal plant defense in Arabidopsis thaliana. The atrav1 mutant lines demonstrate hyper‐susceptibility against fungal pathogens (Rhizoctonia solani and Botrytis cinerea), whereas AtRAV1 overexpressing lines exhibit disease resistance against them. Enhanced expression of various defense genes and activation of mitogen‐activated protein kinases (AtMPK3 and AtMPK6) are observed in the R. solani infected overexpressing lines, but not in the atrav1 mutant plants. An in vitro phosphorylation assay suggests AtRAV1 to be a novel phosphorylation target of AtMPK3. Bimolecular fluorescence complementation and yeast two‐hybrid assays support physical interactions between AtRAV1 and AtMPK3. Overexpression of the native as well as phospho‐mimic but not the phospho‐defective variant of AtRAV1 imparts disease resistance in the atrav1 mutant A. thaliana lines. On the other hand, overexpression of AtRAV1 fails to impart disease resistance in the atmpk3 mutant. These analyses emphasize that AtMPK3‐mediated phosphorylation of AtRAV1 is important for the elaboration of the defense response in A. thaliana. Considering that RAV1 homologs are conserved in diverse plant species, we propose that they can be gainfully deployed to impart disease resistance in agriculturally important crop plants. Indeed, overexpression of SlRAV1 (a member of the RAV1 family) imparts disease tolerance against not only fungal (R. solani and B. cinerea), but also against bacterial (Ralstonia solanacearum) pathogens in tomato, whereas silencing of the gene enhances disease susceptibility.
Significance Statement
AtRAV1 functions as a transcriptional regulator of the defense response in Arabidopsis thaliana and, upon overexpression, it imparts disease resistance. We demonstrate that AtRAV1 transcriptionally regulates mitogen‐activated protein kinases, while AtMPK3 modulates the AtRAV1 function through post‐translational modification (phosphorylation). We provide evidence that SlRAV1 (a member of the RAV1 family) can be gainfully deployed to impart broad‐spectrum disease resistance in tomato.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>36703574</pmid><doi>10.1111/tpj.16114</doi><tpages>54</tpages><orcidid>https://orcid.org/0000-0003-0820-9936</orcidid><orcidid>https://orcid.org/0000-0002-3965-3135</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism bacterial wilt disease Complementation Defense mechanisms Disease control Disease resistance Disease Resistance - genetics Disease tolerance DNA-Binding Proteins - genetics Fungi Gene expression Gene Expression Regulation, Plant Kinases Mitogen-Activated Protein Kinases - metabolism Mutants necrotrophs Pathogens Phosphorylation phytohormone Plant diseases Plant Diseases - genetics Plant Diseases - microbiology Plant immunity Plant species post‐translational modification sheath blight disease Tomatoes Transcription activation transcriptional regulation Yeasts |
title | RAV1 family members function as transcriptional regulators and play a positive role in plant disease resistance |
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