Transcriptome profiling revealed novel transcriptional regulators in maize responses to Ostrinia furnacalis and jasmonic acid
Chewing insects cause severe yield losses in crop production worldwide. Crop plants counteract chewing insects by transcriptionally promoting a repertoire of defense gene products that are either toxic to, or attractive to the natural enemies of, pest insects. However, the complexity of the transcri...
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description | Chewing insects cause severe yield losses in crop production worldwide. Crop plants counteract chewing insects by transcriptionally promoting a repertoire of defense gene products that are either toxic to, or attractive to the natural enemies of, pest insects. However, the complexity of the transcriptional reprogramming in plant defense response against chewing insects is still not well understood. In this study, the genome-wide early responses in maize seedlings to Asian corn borer (ACB, Ostrinia furnacalis) and also to jasmonic acid(JA), the pivotal phytohormone controlling plant defense response against herbivory, were transcriptionally profiled by RNA-Seq. Clustering of differentially expressed genes (DEGs) along with functional enrichment analysis revealed important biological processes regulated in response to ACB infestation and/or jasmonic acid. Moreover, DEGs with distinct expression patterns were differentially enriched with diverse families of cis-elements on their promoters. Multiple inventories of differentially expressed transcription factors (DETFs) in each DEG group were also analyzed. A transient expression assay using transfected maize protoplastswas established to examine the potential roles of DETFs in maize defense response and JA signaling, and this was used to show that ZmNAC60, an ACB- and JA-inducible DETF, represented a novel positive regulator of JA and defense pathway genes. This study provided a comprehensive transcriptional picture for the early dynamics of maize defense responses and JA signaling, and the identification of DETFs offered potential targets for further functional genomics investigation of master regulators in maize defense responses against herbivory. |
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Crop plants counteract chewing insects by transcriptionally promoting a repertoire of defense gene products that are either toxic to, or attractive to the natural enemies of, pest insects. However, the complexity of the transcriptional reprogramming in plant defense response against chewing insects is still not well understood. In this study, the genome-wide early responses in maize seedlings to Asian corn borer (ACB, Ostrinia furnacalis) and also to jasmonic acid(JA), the pivotal phytohormone controlling plant defense response against herbivory, were transcriptionally profiled by RNA-Seq. Clustering of differentially expressed genes (DEGs) along with functional enrichment analysis revealed important biological processes regulated in response to ACB infestation and/or jasmonic acid. Moreover, DEGs with distinct expression patterns were differentially enriched with diverse families of cis-elements on their promoters. Multiple inventories of differentially expressed transcription factors (DETFs) in each DEG group were also analyzed. A transient expression assay using transfected maize protoplastswas established to examine the potential roles of DETFs in maize defense response and JA signaling, and this was used to show that ZmNAC60, an ACB- and JA-inducible DETF, represented a novel positive regulator of JA and defense pathway genes. This study provided a comprehensive transcriptional picture for the early dynamics of maize defense responses and JA signaling, and the identification of DETFs offered potential targets for further functional genomics investigation of master regulators in maize defense responses against herbivory.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0177739</identifier><identifier>PMID: 28520800</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abscisic acid ; Alkaloids ; Allelochemicals ; Animals ; Biology and Life Sciences ; Biotechnology ; Calcium signalling ; Chewing ; Corn ; Corn borers ; Crop production ; Cyclopentanes - pharmacology ; Defense mechanisms ; Depolarization ; DNA binding proteins ; Drought ; Ecology and Environmental Sciences ; Exons ; Gene expression ; Gene Expression Regulation, Plant ; Genetic aspects ; Genomes ; Genomics ; Grain ; Herbivores ; Herbivory ; Insects ; Jasmonates ; Leaves ; Membrane potential ; Metabolites ; Mildew ; Moths - pathogenicity ; Natural enemies ; Oxylipins - pharmacology ; Pathogens ; Perception ; Physiological aspects ; Plant diseases ; Plant hormones ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Promoter Regions, Genetic ; Research and Analysis Methods ; Ribonucleic acid ; Rice ; RNA ; Seedlings ; Signal transduction ; Transcription (Genetics) ; Transcription factors ; Transcription Factors - genetics ; Transcription Factors - metabolism ; Transcriptome ; Zea mays - drug effects ; Zea mays - genetics ; Zea mays - parasitology</subject><ispartof>PloS one, 2017-05, Vol.12 (5), p.e0177739</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Wang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2017 Wang et al 2017 Wang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-7a49d4e769a469b997b888e0fea265591afdfde46e07dd334a35c55027f8f0c23</citedby><cites>FETCH-LOGICAL-c692t-7a49d4e769a469b997b888e0fea265591afdfde46e07dd334a35c55027f8f0c23</cites><orcidid>0000-0003-1927-2447</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5433750/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5433750/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,2103,2929,23871,27929,27930,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28520800$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Aroca, Ricardo</contributor><creatorcontrib>Wang, Hai</creatorcontrib><creatorcontrib>Li, Shengyan</creatorcontrib><creatorcontrib>Teng, Shouzhen</creatorcontrib><creatorcontrib>Liang, Haisheng</creatorcontrib><creatorcontrib>Xin, Hongjia</creatorcontrib><creatorcontrib>Gao, Hongjiang</creatorcontrib><creatorcontrib>Huang, Dafang</creatorcontrib><creatorcontrib>Lang, Zhihong</creatorcontrib><title>Transcriptome profiling revealed novel transcriptional regulators in maize responses to Ostrinia furnacalis and jasmonic acid</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Chewing insects cause severe yield losses in crop production worldwide. Crop plants counteract chewing insects by transcriptionally promoting a repertoire of defense gene products that are either toxic to, or attractive to the natural enemies of, pest insects. However, the complexity of the transcriptional reprogramming in plant defense response against chewing insects is still not well understood. In this study, the genome-wide early responses in maize seedlings to Asian corn borer (ACB, Ostrinia furnacalis) and also to jasmonic acid(JA), the pivotal phytohormone controlling plant defense response against herbivory, were transcriptionally profiled by RNA-Seq. Clustering of differentially expressed genes (DEGs) along with functional enrichment analysis revealed important biological processes regulated in response to ACB infestation and/or jasmonic acid. Moreover, DEGs with distinct expression patterns were differentially enriched with diverse families of cis-elements on their promoters. Multiple inventories of differentially expressed transcription factors (DETFs) in each DEG group were also analyzed. A transient expression assay using transfected maize protoplastswas established to examine the potential roles of DETFs in maize defense response and JA signaling, and this was used to show that ZmNAC60, an ACB- and JA-inducible DETF, represented a novel positive regulator of JA and defense pathway genes. This study provided a comprehensive transcriptional picture for the early dynamics of maize defense responses and JA signaling, and the identification of DETFs offered potential targets for further functional genomics investigation of master regulators in maize defense responses against herbivory.</description><subject>Abscisic acid</subject><subject>Alkaloids</subject><subject>Allelochemicals</subject><subject>Animals</subject><subject>Biology and Life Sciences</subject><subject>Biotechnology</subject><subject>Calcium signalling</subject><subject>Chewing</subject><subject>Corn</subject><subject>Corn borers</subject><subject>Crop production</subject><subject>Cyclopentanes - pharmacology</subject><subject>Defense mechanisms</subject><subject>Depolarization</subject><subject>DNA binding proteins</subject><subject>Drought</subject><subject>Ecology and Environmental Sciences</subject><subject>Exons</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Grain</subject><subject>Herbivores</subject><subject>Herbivory</subject><subject>Insects</subject><subject>Jasmonates</subject><subject>Leaves</subject><subject>Membrane potential</subject><subject>Metabolites</subject><subject>Mildew</subject><subject>Moths - pathogenicity</subject><subject>Natural enemies</subject><subject>Oxylipins - pharmacology</subject><subject>Pathogens</subject><subject>Perception</subject><subject>Physiological aspects</subject><subject>Plant diseases</subject><subject>Plant hormones</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Promoter Regions, Genetic</subject><subject>Research and Analysis Methods</subject><subject>Ribonucleic acid</subject><subject>Rice</subject><subject>RNA</subject><subject>Seedlings</subject><subject>Signal transduction</subject><subject>Transcription (Genetics)</subject><subject>Transcription factors</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>Transcriptome</subject><subject>Zea mays - drug effects</subject><subject>Zea mays - genetics</subject><subject>Zea mays - parasitology</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNkl-LEzEUxQdR3HX1G4gGBMGH1kwyM0leFpbFP4WFgq6-hjS56abMJDWZKSr43U3tbOmAguQhIfndcy8npyiel3heUla-3YQhetXOt8HDHJeMMSoeFOeloGTWEEwfnpzPiicpbTCuKW-ax8UZ4TXBHOPz4tdtVD7p6LZ96ABtY7CudX6NIuxAtWCQDztoUX_EXMhd8_N6aFUfYkLOo065n5DvUh4mQUJ9QMvUR-edQnY_platS0h5gzYqdcE7jZR25mnxyKo2wbNxvyi-vH93e_1xdrP8sLi-upnpRpB-xlQlTAWsEapqxEoItuKcA7agSFPXolTWWANVA5gZQ2mlaK3rGhNmucWa0Ivi5UF324YkR-eSLLkQlDWUl5lYHAgT1EZuo-tU_CGDcvLPRYhrqWLvdAtS1dSa0ghNCKnAEs6FtgCE6UZVZrXXuhy7DasOjAaf3WsnotMX7-7kOuxkXVHKapwFXo0CMXwbIPX_GHmk1vmfpPM2ZDHduaTlVSVKTigjTabmf6HyMtA5nbOT_xumBW8mBZnp4Xu_VkNKcvH50_-zy69T9vUJe5fD1d-l0A77QKUpWB1AHUNKEezRuRLLffTv3ZD76Msx-rnsxanrx6L7rNPfGq0CjQ</recordid><startdate>20170516</startdate><enddate>20170516</enddate><creator>Wang, Hai</creator><creator>Li, Shengyan</creator><creator>Teng, Shouzhen</creator><creator>Liang, Haisheng</creator><creator>Xin, Hongjia</creator><creator>Gao, Hongjiang</creator><creator>Huang, Dafang</creator><creator>Lang, Zhihong</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0003-1927-2447</orcidid></search><sort><creationdate>20170516</creationdate><title>Transcriptome profiling revealed novel transcriptional regulators in maize responses to Ostrinia furnacalis and jasmonic acid</title><author>Wang, Hai ; Li, Shengyan ; Teng, Shouzhen ; Liang, Haisheng ; Xin, Hongjia ; Gao, Hongjiang ; Huang, Dafang ; Lang, Zhihong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-7a49d4e769a469b997b888e0fea265591afdfde46e07dd334a35c55027f8f0c23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Abscisic acid</topic><topic>Alkaloids</topic><topic>Allelochemicals</topic><topic>Animals</topic><topic>Biology and Life Sciences</topic><topic>Biotechnology</topic><topic>Calcium signalling</topic><topic>Chewing</topic><topic>Corn</topic><topic>Corn borers</topic><topic>Crop production</topic><topic>Cyclopentanes - pharmacology</topic><topic>Defense mechanisms</topic><topic>Depolarization</topic><topic>DNA binding proteins</topic><topic>Drought</topic><topic>Ecology and Environmental Sciences</topic><topic>Exons</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genetic aspects</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Grain</topic><topic>Herbivores</topic><topic>Herbivory</topic><topic>Insects</topic><topic>Jasmonates</topic><topic>Leaves</topic><topic>Membrane potential</topic><topic>Metabolites</topic><topic>Mildew</topic><topic>Moths - pathogenicity</topic><topic>Natural enemies</topic><topic>Oxylipins - pharmacology</topic><topic>Pathogens</topic><topic>Perception</topic><topic>Physiological aspects</topic><topic>Plant diseases</topic><topic>Plant hormones</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Promoter Regions, Genetic</topic><topic>Research and Analysis Methods</topic><topic>Ribonucleic acid</topic><topic>Rice</topic><topic>RNA</topic><topic>Seedlings</topic><topic>Signal transduction</topic><topic>Transcription (Genetics)</topic><topic>Transcription factors</topic><topic>Transcription Factors - 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Crop plants counteract chewing insects by transcriptionally promoting a repertoire of defense gene products that are either toxic to, or attractive to the natural enemies of, pest insects. However, the complexity of the transcriptional reprogramming in plant defense response against chewing insects is still not well understood. In this study, the genome-wide early responses in maize seedlings to Asian corn borer (ACB, Ostrinia furnacalis) and also to jasmonic acid(JA), the pivotal phytohormone controlling plant defense response against herbivory, were transcriptionally profiled by RNA-Seq. Clustering of differentially expressed genes (DEGs) along with functional enrichment analysis revealed important biological processes regulated in response to ACB infestation and/or jasmonic acid. Moreover, DEGs with distinct expression patterns were differentially enriched with diverse families of cis-elements on their promoters. Multiple inventories of differentially expressed transcription factors (DETFs) in each DEG group were also analyzed. A transient expression assay using transfected maize protoplastswas established to examine the potential roles of DETFs in maize defense response and JA signaling, and this was used to show that ZmNAC60, an ACB- and JA-inducible DETF, represented a novel positive regulator of JA and defense pathway genes. This study provided a comprehensive transcriptional picture for the early dynamics of maize defense responses and JA signaling, and the identification of DETFs offered potential targets for further functional genomics investigation of master regulators in maize defense responses against herbivory.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28520800</pmid><doi>10.1371/journal.pone.0177739</doi><tpages>e0177739</tpages><orcidid>https://orcid.org/0000-0003-1927-2447</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Abscisic acid Alkaloids Allelochemicals Animals Biology and Life Sciences Biotechnology Calcium signalling Chewing Corn Corn borers Crop production Cyclopentanes - pharmacology Defense mechanisms Depolarization DNA binding proteins Drought Ecology and Environmental Sciences Exons Gene expression Gene Expression Regulation, Plant Genetic aspects Genomes Genomics Grain Herbivores Herbivory Insects Jasmonates Leaves Membrane potential Metabolites Mildew Moths - pathogenicity Natural enemies Oxylipins - pharmacology Pathogens Perception Physiological aspects Plant diseases Plant hormones Plant Proteins - genetics Plant Proteins - metabolism Promoter Regions, Genetic Research and Analysis Methods Ribonucleic acid Rice RNA Seedlings Signal transduction Transcription (Genetics) Transcription factors Transcription Factors - genetics Transcription Factors - metabolism Transcriptome Zea mays - drug effects Zea mays - genetics Zea mays - parasitology |
title | Transcriptome profiling revealed novel transcriptional regulators in maize responses to Ostrinia furnacalis and jasmonic acid |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-12T21%3A49%3A11IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Transcriptome%20profiling%20revealed%20novel%20transcriptional%20regulators%20in%20maize%20responses%20to%20Ostrinia%20furnacalis%20and%20jasmonic%20acid&rft.jtitle=PloS%20one&rft.au=Wang,%20Hai&rft.date=2017-05-16&rft.volume=12&rft.issue=5&rft.spage=e0177739&rft.pages=e0177739-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0177739&rft_dat=%3Cgale_plos_%3EA491823726%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1899376381&rft_id=info:pmid/28520800&rft_galeid=A491823726&rft_doaj_id=oai_doaj_org_article_a53fd1d9c2224ef2889cfee27c6a4db1&rfr_iscdi=true |