Endophytic Fungi‐Mediated Defense Signaling in Maize: Unraveling the Role of WRKY36 in Regulating Immunity against Spodoptera frugiperda
Seed priming with beneficial endophytic fungi is an emerging sustainable strategy for enhancing plant resistance against insect pests. This study examined the effects of Beauvaria bassiana Bb20091317 and Metarhizium rileyi MrCDTLJ1 fungal colonization on maize growth, defence signalling, benzoxazino...
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| Veröffentlicht in: | Physiologia plantarum 2024-03, Vol.176 (2), p.e14243-n/a |
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| creator | Batool, Raufa Xuelian, Gou Hui, Dong Xiuzhen, Long Umer, Muhammad Jawad Rwomushana, Ivan Ali, Abid Attia, Kotb A. Jingfei, Guo Zhenying, Wang |
| description | Seed priming with beneficial endophytic fungi is an emerging sustainable strategy for enhancing plant resistance against insect pests. This study examined the effects of Beauvaria bassiana Bb20091317 and Metarhizium rileyi MrCDTLJ1 fungal colonization on maize growth, defence signalling, benzoxazinoid levels and gene expression. The colonization did not adversely affect plant growth but reduced larval weights of Spodoptera frugiperda. Maize leaves treated with M. rileyi exhibited higher levels of jasmonic acid, jasmonoyl‐Isoleucine, salicylic acid, and indole acetic acid compared to control. B. bassiana and M. rileyi accelerated phytohormone increase upon S. frugiperda herbivory. Gene expression analysis revealed modulation of benzoxazinoid biosynthesis genes. We further elucidated the immune regulatory role of the transcription factor zmWRKY36 using virus‐induced gene silencing (VIGS) in maize. zmWRKY36 positively regulates maize immunity against S. frugiperda, likely by interacting with defense‐related proteins. Transient overexpression of zmWRKY36 in tobacco‐induced cell death, while silencing in maize reduced chitin‐triggered reactive oxygen species burst, confirming its immune function. Overall, B. bassiana and M. rileyi successfully colonized maize, impacting larval growth, defense signalling, and zmWRKY36‐mediated resistance. This sheds light on maize‐endophyte‐insect interactions for sustainable plant protection. |
| doi_str_mv | 10.1111/ppl.14243 |
| format | Article |
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This study examined the effects of Beauvaria bassiana Bb20091317 and Metarhizium rileyi MrCDTLJ1 fungal colonization on maize growth, defence signalling, benzoxazinoid levels and gene expression. The colonization did not adversely affect plant growth but reduced larval weights of Spodoptera frugiperda. Maize leaves treated with M. rileyi exhibited higher levels of jasmonic acid, jasmonoyl‐Isoleucine, salicylic acid, and indole acetic acid compared to control. B. bassiana and M. rileyi accelerated phytohormone increase upon S. frugiperda herbivory. Gene expression analysis revealed modulation of benzoxazinoid biosynthesis genes. We further elucidated the immune regulatory role of the transcription factor zmWRKY36 using virus‐induced gene silencing (VIGS) in maize. zmWRKY36 positively regulates maize immunity against S. frugiperda, likely by interacting with defense‐related proteins. Transient overexpression of zmWRKY36 in tobacco‐induced cell death, while silencing in maize reduced chitin‐triggered reactive oxygen species burst, confirming its immune function. Overall, B. bassiana and M. rileyi successfully colonized maize, impacting larval growth, defense signalling, and zmWRKY36‐mediated resistance. This sheds light on maize‐endophyte‐insect interactions for sustainable plant protection.</description><identifier>ISSN: 0031-9317</identifier><identifier>EISSN: 1399-3054</identifier><identifier>DOI: 10.1111/ppl.14243</identifier><identifier>PMID: 38467539</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Acetic acid ; Animals ; Bassiana ; Benzoxazines - metabolism ; Benzoxazines - pharmacology ; Biosynthesis ; Cell death ; Chitin ; Colonization ; Corn ; Endophytes ; Fungi ; Gene expression ; Gene silencing ; genes ; herbivores ; Herbivory ; Immune response ; Immunity ; indole acetic acid ; Indoleacetic acid ; Insects ; Isoleucine ; Jasmonic acid ; Larva - physiology ; larvae ; Larval development ; Metarhizium ; Pest resistance ; Pests ; Plant growth ; Plant hormones ; Plant protection ; Plant resistance ; Reactive oxygen species ; Salicylic acid ; Spodoptera - physiology ; Spodoptera frugiperda ; Tobacco ; transcription factors ; Zea mays - genetics ; Zea mays - metabolism</subject><ispartof>Physiologia plantarum, 2024-03, Vol.176 (2), p.e14243-n/a</ispartof><rights>2024 Scandinavian Plant Physiology Society.</rights><rights>2024 Scandinavian Plant Physiology Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3863-4410531fbb2fa0f693c385507c1467ebfa90cbe0d372e26af1f80b0cb204da193</citedby><cites>FETCH-LOGICAL-c3863-4410531fbb2fa0f693c385507c1467ebfa90cbe0d372e26af1f80b0cb204da193</cites><orcidid>0000-0003-2043-0684 ; 0000-0002-7514-9227</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%2Fppl.14243$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fppl.14243$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38467539$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Batool, Raufa</creatorcontrib><creatorcontrib>Xuelian, Gou</creatorcontrib><creatorcontrib>Hui, Dong</creatorcontrib><creatorcontrib>Xiuzhen, Long</creatorcontrib><creatorcontrib>Umer, Muhammad Jawad</creatorcontrib><creatorcontrib>Rwomushana, Ivan</creatorcontrib><creatorcontrib>Ali, Abid</creatorcontrib><creatorcontrib>Attia, Kotb A.</creatorcontrib><creatorcontrib>Jingfei, Guo</creatorcontrib><creatorcontrib>Zhenying, Wang</creatorcontrib><title>Endophytic Fungi‐Mediated Defense Signaling in Maize: Unraveling the Role of WRKY36 in Regulating Immunity against Spodoptera frugiperda</title><title>Physiologia plantarum</title><addtitle>Physiol Plant</addtitle><description>Seed priming with beneficial endophytic fungi is an emerging sustainable strategy for enhancing plant resistance against insect pests. This study examined the effects of Beauvaria bassiana Bb20091317 and Metarhizium rileyi MrCDTLJ1 fungal colonization on maize growth, defence signalling, benzoxazinoid levels and gene expression. The colonization did not adversely affect plant growth but reduced larval weights of Spodoptera frugiperda. Maize leaves treated with M. rileyi exhibited higher levels of jasmonic acid, jasmonoyl‐Isoleucine, salicylic acid, and indole acetic acid compared to control. B. bassiana and M. rileyi accelerated phytohormone increase upon S. frugiperda herbivory. Gene expression analysis revealed modulation of benzoxazinoid biosynthesis genes. We further elucidated the immune regulatory role of the transcription factor zmWRKY36 using virus‐induced gene silencing (VIGS) in maize. zmWRKY36 positively regulates maize immunity against S. frugiperda, likely by interacting with defense‐related proteins. Transient overexpression of zmWRKY36 in tobacco‐induced cell death, while silencing in maize reduced chitin‐triggered reactive oxygen species burst, confirming its immune function. Overall, B. bassiana and M. rileyi successfully colonized maize, impacting larval growth, defense signalling, and zmWRKY36‐mediated resistance. This sheds light on maize‐endophyte‐insect interactions for sustainable plant protection.</description><subject>Acetic acid</subject><subject>Animals</subject><subject>Bassiana</subject><subject>Benzoxazines - metabolism</subject><subject>Benzoxazines - pharmacology</subject><subject>Biosynthesis</subject><subject>Cell death</subject><subject>Chitin</subject><subject>Colonization</subject><subject>Corn</subject><subject>Endophytes</subject><subject>Fungi</subject><subject>Gene expression</subject><subject>Gene silencing</subject><subject>genes</subject><subject>herbivores</subject><subject>Herbivory</subject><subject>Immune response</subject><subject>Immunity</subject><subject>indole acetic acid</subject><subject>Indoleacetic acid</subject><subject>Insects</subject><subject>Isoleucine</subject><subject>Jasmonic acid</subject><subject>Larva - physiology</subject><subject>larvae</subject><subject>Larval development</subject><subject>Metarhizium</subject><subject>Pest resistance</subject><subject>Pests</subject><subject>Plant growth</subject><subject>Plant hormones</subject><subject>Plant protection</subject><subject>Plant resistance</subject><subject>Reactive oxygen species</subject><subject>Salicylic acid</subject><subject>Spodoptera - physiology</subject><subject>Spodoptera frugiperda</subject><subject>Tobacco</subject><subject>transcription factors</subject><subject>Zea mays - genetics</subject><subject>Zea mays - metabolism</subject><issn>0031-9317</issn><issn>1399-3054</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc1u1DAURi0EokNhwQsgS2zKIq1v7DgxO9QfqJiKakqFWEVOcp26SpxgJ62GFWtWPCNPgqdTWCAhvLnSp6Nz5fsR8hzYPsR3MI7dPohU8AdkAVyphLNMPCQLxjgkikO-Q56EcM0YSAnpY7LDCyHzjKsF-X7smmG8Wk-2pieza-3Pbz_OsLF6woYeoUEXkF7Y1unOupZaR8-0_Yqv6aXz-gbvwukK6WrokA6Gflq9_8zlhlthO3d62gCnfT87O62pbrV1YaIX4xC3Tug1NX5u7Yi-0U_JI6O7gM_u5y65PDn-ePguWX54e3r4ZpnUvJA8EQJYxsFUVWo0M1LxmGcZy2uIn8LKaMXqClnD8xRTqQ2YglUxSploNCi-S_a23tEPX2YMU9nbUGPXaYfDHEoOUa-4lMV_0VRlEjIlgUf05V_o9TD7eLYoZEIUeQosj9SrLVX7IQSPphy97bVfl8DKTZdl7LK86zKyL-6Nc9Vj84f8XV4EDrbAre1w_W9TeX6-3Cp_AQ7UqTY</recordid><startdate>202403</startdate><enddate>202403</enddate><creator>Batool, Raufa</creator><creator>Xuelian, Gou</creator><creator>Hui, Dong</creator><creator>Xiuzhen, Long</creator><creator>Umer, Muhammad Jawad</creator><creator>Rwomushana, Ivan</creator><creator>Ali, Abid</creator><creator>Attia, Kotb A.</creator><creator>Jingfei, Guo</creator><creator>Zhenying, Wang</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</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>7SN</scope><scope>7ST</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0003-2043-0684</orcidid><orcidid>https://orcid.org/0000-0002-7514-9227</orcidid></search><sort><creationdate>202403</creationdate><title>Endophytic Fungi‐Mediated Defense Signaling in Maize: Unraveling the Role of WRKY36 in Regulating Immunity against Spodoptera frugiperda</title><author>Batool, Raufa ; Xuelian, Gou ; Hui, Dong ; Xiuzhen, Long ; Umer, Muhammad Jawad ; Rwomushana, Ivan ; Ali, Abid ; Attia, Kotb A. ; Jingfei, Guo ; Zhenying, Wang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3863-4410531fbb2fa0f693c385507c1467ebfa90cbe0d372e26af1f80b0cb204da193</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Acetic acid</topic><topic>Animals</topic><topic>Bassiana</topic><topic>Benzoxazines - metabolism</topic><topic>Benzoxazines - pharmacology</topic><topic>Biosynthesis</topic><topic>Cell death</topic><topic>Chitin</topic><topic>Colonization</topic><topic>Corn</topic><topic>Endophytes</topic><topic>Fungi</topic><topic>Gene expression</topic><topic>Gene silencing</topic><topic>genes</topic><topic>herbivores</topic><topic>Herbivory</topic><topic>Immune response</topic><topic>Immunity</topic><topic>indole acetic acid</topic><topic>Indoleacetic acid</topic><topic>Insects</topic><topic>Isoleucine</topic><topic>Jasmonic acid</topic><topic>Larva - physiology</topic><topic>larvae</topic><topic>Larval development</topic><topic>Metarhizium</topic><topic>Pest resistance</topic><topic>Pests</topic><topic>Plant growth</topic><topic>Plant hormones</topic><topic>Plant protection</topic><topic>Plant resistance</topic><topic>Reactive oxygen species</topic><topic>Salicylic acid</topic><topic>Spodoptera - physiology</topic><topic>Spodoptera frugiperda</topic><topic>Tobacco</topic><topic>transcription factors</topic><topic>Zea mays - genetics</topic><topic>Zea mays - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Batool, Raufa</creatorcontrib><creatorcontrib>Xuelian, Gou</creatorcontrib><creatorcontrib>Hui, Dong</creatorcontrib><creatorcontrib>Xiuzhen, Long</creatorcontrib><creatorcontrib>Umer, Muhammad Jawad</creatorcontrib><creatorcontrib>Rwomushana, Ivan</creatorcontrib><creatorcontrib>Ali, Abid</creatorcontrib><creatorcontrib>Attia, Kotb A.</creatorcontrib><creatorcontrib>Jingfei, Guo</creatorcontrib><creatorcontrib>Zhenying, Wang</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Environment Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Physiologia plantarum</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Batool, Raufa</au><au>Xuelian, Gou</au><au>Hui, Dong</au><au>Xiuzhen, Long</au><au>Umer, Muhammad Jawad</au><au>Rwomushana, Ivan</au><au>Ali, Abid</au><au>Attia, Kotb A.</au><au>Jingfei, Guo</au><au>Zhenying, Wang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Endophytic Fungi‐Mediated Defense Signaling in Maize: Unraveling the Role of WRKY36 in Regulating Immunity against Spodoptera frugiperda</atitle><jtitle>Physiologia plantarum</jtitle><addtitle>Physiol Plant</addtitle><date>2024-03</date><risdate>2024</risdate><volume>176</volume><issue>2</issue><spage>e14243</spage><epage>n/a</epage><pages>e14243-n/a</pages><issn>0031-9317</issn><eissn>1399-3054</eissn><abstract>Seed priming with beneficial endophytic fungi is an emerging sustainable strategy for enhancing plant resistance against insect pests. This study examined the effects of Beauvaria bassiana Bb20091317 and Metarhizium rileyi MrCDTLJ1 fungal colonization on maize growth, defence signalling, benzoxazinoid levels and gene expression. The colonization did not adversely affect plant growth but reduced larval weights of Spodoptera frugiperda. Maize leaves treated with M. rileyi exhibited higher levels of jasmonic acid, jasmonoyl‐Isoleucine, salicylic acid, and indole acetic acid compared to control. B. bassiana and M. rileyi accelerated phytohormone increase upon S. frugiperda herbivory. Gene expression analysis revealed modulation of benzoxazinoid biosynthesis genes. We further elucidated the immune regulatory role of the transcription factor zmWRKY36 using virus‐induced gene silencing (VIGS) in maize. zmWRKY36 positively regulates maize immunity against S. frugiperda, likely by interacting with defense‐related proteins. Transient overexpression of zmWRKY36 in tobacco‐induced cell death, while silencing in maize reduced chitin‐triggered reactive oxygen species burst, confirming its immune function. Overall, B. bassiana and M. rileyi successfully colonized maize, impacting larval growth, defense signalling, and zmWRKY36‐mediated resistance. This sheds light on maize‐endophyte‐insect interactions for sustainable plant protection.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>38467539</pmid><doi>10.1111/ppl.14243</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0003-2043-0684</orcidid><orcidid>https://orcid.org/0000-0002-7514-9227</orcidid></addata></record> |
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| subjects | Acetic acid Animals Bassiana Benzoxazines - metabolism Benzoxazines - pharmacology Biosynthesis Cell death Chitin Colonization Corn Endophytes Fungi Gene expression Gene silencing genes herbivores Herbivory Immune response Immunity indole acetic acid Indoleacetic acid Insects Isoleucine Jasmonic acid Larva - physiology larvae Larval development Metarhizium Pest resistance Pests Plant growth Plant hormones Plant protection Plant resistance Reactive oxygen species Salicylic acid Spodoptera - physiology Spodoptera frugiperda Tobacco transcription factors Zea mays - genetics Zea mays - metabolism |
| title | Endophytic Fungi‐Mediated Defense Signaling in Maize: Unraveling the Role of WRKY36 in Regulating Immunity against Spodoptera frugiperda |
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