{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T22:26:55Z","timestamp":1791412015711,"version":"4.3.3"},"reference-count":89,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2007,9,20]],"date-time":"2007-09-20T00:00:00Z","timestamp":1190246400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2007,11,5]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>We have previously shown that the beneficial filamentous fungus Trichoderma virens secretes the highly effective hydrophobin-like elicitor Sm1 that induces systemic disease resistance in the dicot cotton (Gossypium hirsutum). In this study we tested whether colonization of roots by T. virens can induce systemic protection against a foliar pathogen in the monocot maize (Zea mays), and we further demonstrated the importance of Sm1 during maize-fungal interactions using a functional genomics approach. Maize seedlings were inoculated with T. virens Gv29-8 wild type and transformants in which SM1 was disrupted or constitutively overexpressed in a hydroponic system or in soil-grown maize seedlings challenged with the pathogen Colletotrichum graminicola. We show that similar to dicot plants, colonization of maize roots by T. virens induces systemic protection of the leaves inoculated with C. graminicola. This protection was associated with notable induction of jasmonic acid- and green leaf volatile-biosynthetic genes. Neither deletion nor overexpression of SM1 affected normal growth or development of T. virens, conidial germination, production of gliotoxin, hyphal coiling, hydrophobicity, or the ability to colonize maize roots. Plant bioassays showed that maize grown with SM1-deletion strains exhibited the same levels of systemic protection as non-Trichoderma-treated plants. Moreover, deletion and overexpression of SM1 resulted in significantly reduced and enhanced levels of disease protection, respectively, compared to the wild type. These data together indicate that T. virens is able to effectively activate systemic disease protection in maize and that the functional Sm1 elicitor is required for this activity.<\/jats:p>","DOI":"10.1104\/pp.107.103689","type":"journal-article","created":{"date-parts":[[2007,9,20]],"date-time":"2007-09-20T20:59:08Z","timestamp":1190321948000},"page":"875-889","source":"Crossref","is-referenced-by-count":295,"title":["A Proteinaceous Elicitor Sm1 from the Beneficial Fungus\n                    <i>Trichoderma virens<\/i>\n                    Is Required for Induced Systemic Resistance in Maize"],"prefix":"10.1093","volume":"145","author":[{"given":"Slavica","family":"Djonovic\u0301","sequence":"first","affiliation":[{"name":"Department of Plant Pathology and Microbiology, Texas A&M University, College Station, Texas 77843"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Walter A.","family":"Vargas","sequence":"additional","affiliation":[{"name":"Department of Plant Pathology and Microbiology, Texas A&M University, College Station, Texas 77843"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael V.","family":"Kolomiets","sequence":"additional","affiliation":[{"name":"Department of Plant Pathology and Microbiology, Texas A&M University, College Station, Texas 77843"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michelle","family":"Horndeski","sequence":"additional","affiliation":[{"name":"Department of Plant Pathology and Microbiology, Texas A&M University, College Station, Texas 77843"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aric","family":"Wiest","sequence":"additional","affiliation":[{"name":"Department of Plant Pathology and Microbiology, Texas A&M University, College Station, Texas 77843"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Charles M.","family":"Kenerley","sequence":"additional","affiliation":[{"name":"Department of Plant Pathology and Microbiology, Texas A&M University, College Station, Texas 77843"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2007,9,20]]},"reference":[{"key":"2021041513065312300_b1","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1006\/bbrc.2000.3114","volume":"274","year":"2000","journal-title":"Biochem Biophys Res Commun"},{"key":"2021041513065312300_b2","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1006\/fgbi.1997.1025","volume":"23","year":"1998","journal-title":"Fungal Genet Biol"},{"key":"2021041513065312300_b3","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1104\/pp.100.2.749","volume":"100","year":"1992","journal-title":"Plant Physiol"},{"key":"2021041513065312300_b4","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.tplants.2003.11.008","volume":"9","year":"2004","journal-title":"Trends Plant Sci"},{"key":"2021041513065312300_b5","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1046\/j.1365-313x.1998.00324.x","volume":"16","year":"1998","journal-title":"Plant J"},{"key":"2021041513065312300_b6","first-page":"249","volume":"7","year":"2004","journal-title":"Int Microbiol"},{"key":"2021041513065312300_b7","doi-asserted-by":"crossref","first-page":"9329","DOI":"10.1073\/pnas.160241697","volume":"97","year":"2000","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021041513065312300_b8","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1111\/j.1574-6968.2004.tb09501.x","volume":"233","year":"2004","journal-title":"FEMS Microbiol Lett"},{"key":"2021041513065312300_b9","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1111\/j.1469-8137.1993.tb03836.x","volume":"124","year":"1993","journal-title":"New Phytol"},{"key":"2021041513065312300_b10","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1094\/MPMI-18-0511","volume":"18","year":"2005","journal-title":"Mol Plant Microbe Interact"},{"key":"2021041513065312300_b11","doi-asserted-by":"crossref","first-page":"1062","DOI":"10.1094\/MPMI-19-1062","volume":"19","year":"2006","journal-title":"Mol Plant Microbe Interact"},{"key":"2021041513065312300_b12","doi-asserted-by":"crossref","first-page":"352","DOI":"10.1007\/BF00221231","volume":"41","year":"1994","journal-title":"Appl Microbiol Biotechnol"},{"key":"2021041513065312300_b13","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1007\/BF00039557","volume":"26","year":"1994","journal-title":"Plant Mol Biol"},{"key":"2021041513065312300_b14","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1046\/j.1364-3703.2002.00131.x","volume":"3","year":"2002","journal-title":"Mol Plant Pathol"},{"key":"2021041513065312300_b15","doi-asserted-by":"crossref","first-page":"838","DOI":"10.1094\/MPMI-19-0838","volume":"19","year":"2006","journal-title":"Mol Plant Microbe Interact"},{"key":"2021041513065312300_b16","doi-asserted-by":"crossref","first-page":"7661","DOI":"10.1128\/AEM.01607-06","volume":"72","year":"2006","journal-title":"Appl Environ Microbiol"},{"key":"2021041513065312300_b17","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1111\/j.1364-3703.2007.00407.x","volume":"8","year":"2007","journal-title":"Mol Plant Pathol"},{"key":"2021041513065312300_b18","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/S1369-5266(00)00178-3","volume":"4","year":"2001","journal-title":"Curr Opin Plant Biol"},{"key":"2021041513065312300_b19","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1016\/j.pbi.2004.07.005","volume":"7","year":"2004","journal-title":"Curr Opin Plant Biol"},{"key":"2021041513065312300_b20","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1111\/j.1469-8137.2004.01248.x","volume":"165","year":"2005","journal-title":"New Phytol"},{"key":"2021041513065312300_b21","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1146\/annurev.phyto.42.040803.140421","volume":"42","year":"2004","journal-title":"Annu Rev Phytopathol"},{"key":"2021041513065312300_b22","doi-asserted-by":"crossref","first-page":"900","DOI":"10.1007\/s00425-004-1404-5","volume":"220","year":"2005","journal-title":"Planta"},{"key":"2021041513065312300_b23","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1146\/annurev.arplant.53.100301.135248","volume":"53","year":"2002","journal-title":"Annu Rev Plant Biol"},{"key":"2021041513065312300_b24","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1104\/pp.121.2.345","volume":"121","year":"1999","journal-title":"Plant Physiol"},{"key":"2021041513065312300_b25","year":"2007"},{"key":"2021041513065312300_b26","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1146\/annurev.phyto.43.040204.135923","volume":"43","year":"2005","journal-title":"Annu Rev Phytopathol"},{"key":"2021041513065312300_b27","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1046\/j.1365-313X.2003.01717.x","volume":"34","year":"2003","journal-title":"Plant J"},{"key":"2021041513065312300_b28","doi-asserted-by":"crossref","first-page":"4487","DOI":"10.1021\/jf030025s","volume":"51","year":"2003","journal-title":"J Agric Food Chem"},{"key":"2021041513065312300_b29","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1094\/PHYTO.2004.94.2.171","volume":"94","year":"2004","journal-title":"Phytopathology"},{"key":"2021041513065312300_b30","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1038\/nrmicro797","volume":"2","year":"2004","journal-title":"Nat Rev Microbiol"},{"key":"2021041513065312300_b31","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1094\/PHYTO.2004.94.2.147","volume":"94","year":"2004","journal-title":"Phytopathology"},{"key":"2021041513065312300_b32","doi-asserted-by":"crossref","first-page":"870","DOI":"10.1093\/pcp\/pci092","volume":"46","year":"2005","journal-title":"Plant Cell Physiol"},{"key":"2021041513065312300_b33","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1023\/A:1026592509060","volume":"44","year":"2000","journal-title":"Plant Mol Biol"},{"key":"2021041513065312300_b34","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1093\/aob\/mcf076","volume":"89","year":"2002","journal-title":"Ann Bot (Lond)"},{"key":"2021041513065312300_b35","doi-asserted-by":"crossref","first-page":"5467","DOI":"10.1073\/pnas.0610266104","volume":"104","year":"2007","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021041513065312300_b36","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1146\/annurev.pp.42.060191.003005","volume":"42","year":"1991","journal-title":"Annu Rev Plant Physiol Plant Mol Biol"},{"key":"2021041513065312300_b37","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1094\/PHYTO.2000.90.3.248","volume":"90","year":"2000","journal-title":"Phytopathology"},{"key":"2021041513065312300_b38","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/S1049-9644(02)00185-8","volume":"27","year":"2003","journal-title":"Biol Control"},{"key":"2021041513065312300_b39","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1093\/pcp\/41.4.440","volume":"41","year":"2000","journal-title":"Plant Cell Physiol"},{"key":"2021041513065312300_b40","doi-asserted-by":"crossref","first-page":"1269","DOI":"10.1104\/pp.106.4.1269","volume":"106","year":"1994","journal-title":"Plant Physiol"},{"key":"2021041513065312300_b41","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.plaphy.2004.10.005","volume":"43","year":"2005","journal-title":"Plant Physiol Biochem"},{"key":"2021041513065312300_b42","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1016\/j.pbi.2006.03.002","volume":"9","year":"2006","journal-title":"Curr Opin Plant Biol"},{"key":"2021041513065312300_b43","doi-asserted-by":"crossref","first-page":"1127","DOI":"10.1094\/MPMI-19-1127","volume":"19","year":"2006","journal-title":"Mol Plant Microbe Interact"},{"key":"2021041513065312300_b44","doi-asserted-by":"crossref","first-page":"490","DOI":"10.1016\/j.tplants.2004.08.009","volume":"9","year":"2004","journal-title":"Trends Plant Sci"},{"key":"2021041513065312300_b45","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1094\/MPMI.1998.11.7.643","volume":"11","year":"1998","journal-title":"Mol Plant Microbe Interact"},{"key":"2021041513065312300_b46","doi-asserted-by":"crossref","first-page":"3767","DOI":"10.1093\/jxb\/erl137","volume":"57","year":"2006","journal-title":"J Exp Bot"},{"key":"2021041513065312300_b47","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1146\/annurev.py.30.090192.002101","volume":"30","year":"1992","journal-title":"Annu Rev Phytopathol"},{"key":"2021041513065312300_b48","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1146\/annurev.genet.37.110801.142628","volume":"37","year":"2003","journal-title":"Annu Rev Genet"},{"key":"2021041513065312300_b49","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.1094\/MPMI.2004.17.9.1009","volume":"17","year":"2004","journal-title":"Mol Plant Microbe Interact"},{"key":"2021041513065312300_b50","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1007\/BF00172638","volume":"23","year":"1992","journal-title":"Microb Ecol"},{"key":"2021041513065312300_b51","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1016\/S1360-1385(00)01603-4","volume":"5","year":"2000","journal-title":"Trends Plant Sci"},{"key":"2021041513065312300_b52","doi-asserted-by":"crossref","first-page":"24959","DOI":"10.1074\/jbc.274.35.24959","volume":"274","year":"1999","journal-title":"J Biol Chem"},{"key":"2021041513065312300_b53","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/S1360-1385(98)01364-8","volume":"4","year":"1999","journal-title":"Trends Plant Sci"},{"key":"2021041513065312300_b54","first-page":"39","volume":"35","year":"2003","journal-title":"Symbiosis"},{"key":"2021041513065312300_b55","first-page":"211","volume":"23","year":"2005","journal-title":"J Plant Growth Regul"},{"key":"2021041513065312300_b56","doi-asserted-by":"crossref","first-page":"2492","DOI":"10.1002\/1522-2683(20000701)21:12<2492::AID-ELPS2492>3.0.CO;2-2","volume":"21","year":"2000","journal-title":"Electrophoresis"},{"key":"2021041513065312300_b57","doi-asserted-by":"crossref","first-page":"1049","DOI":"10.1046\/j.1365-313X.2002.01490.x","volume":"32","year":"2002","journal-title":"Plant J"},{"key":"2021041513065312300_b58","year":"1989"},{"key":"2021041513065312300_b59","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1094\/MPMI.1997.10.6.779","volume":"10","year":"1997","journal-title":"Mol Plant Microbe Interact"},{"key":"2021041513065312300_b60","doi-asserted-by":"crossref","first-page":"11655","DOI":"10.1073\/pnas.97.21.11655","volume":"97","year":"2000","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021041513065312300_b61","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1006\/fgbi.2000.1205","volume":"30","year":"2000","journal-title":"Fungal Genet Biol"},{"key":"2021041513065312300_b62","doi-asserted-by":"crossref","first-page":"659","DOI":"10.1023\/A:1008791223608","volume":"105","year":"1999","journal-title":"Eur J Plant Pathol"},{"key":"2021041513065312300_b63","doi-asserted-by":"crossref","first-page":"16672","DOI":"10.1073\/pnas.0607780103","volume":"103","year":"2006","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021041513065312300_b64","doi-asserted-by":"crossref","first-page":"1169","DOI":"10.1104\/pp.106.082107","volume":"142","year":"2006","journal-title":"Plant Physiol"},{"key":"2021041513065312300_b65","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1094\/PHYTO-95-0076","volume":"95","year":"2005","journal-title":"Phytopathology"},{"key":"2021041513065312300_b66","first-page":"79","volume":"36","year":"1989","journal-title":"Fungal Genet Newsl"},{"key":"2021041513065312300_b67","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1023\/A:1020235916345","volume":"244","year":"2002","journal-title":"Plant Soil"},{"key":"2021041513065312300_b68","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/0378-1119(95)00725-3","volume":"168","year":"1996","journal-title":"Gene"},{"key":"2021041513065312300_b69","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1007\/BF00376798","volume":"15","year":"1989","journal-title":"Curr Genet"},{"key":"2021041513065312300_b70","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1094\/MPMI.2002.15.1.27","volume":"15","year":"2002","journal-title":"Mol Plant Microbe Interact"},{"key":"2021041513065312300_b71","doi-asserted-by":"crossref","first-page":"S153","DOI":"10.1105\/tpc.000679","volume":"14","year":"2002","journal-title":"Plant Cell (Suppl)"},{"key":"2021041513065312300_b72","year":"1991"},{"key":"2021041513065312300_b73","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1146\/annurev.phyto.36.1.453","volume":"36","year":"1998","journal-title":"Annu Rev Phytopathol"},{"key":"2021041513065312300_b74","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1006\/pmpp.1999.0213","volume":"55","year":"1999","journal-title":"Physiol Mol Plant Pathol"},{"key":"2021041513065312300_b75","doi-asserted-by":"crossref","first-page":"686","DOI":"10.2144\/97234st01","volume":"23","year":"1997","journal-title":"Biotechniques"},{"key":"2021041513065312300_b76","doi-asserted-by":"crossref","first-page":"1580","DOI":"10.1104\/pp.102.013417","volume":"131","year":"2003","journal-title":"Plant Physiol"},{"key":"2021041513065312300_b77","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1111\/j.1364-3703.2006.00335.x","volume":"7","year":"2006","journal-title":"Mol Plant Pathol"},{"key":"2021041513065312300_b78","first-page":"151","volume":"238","year":"2004","journal-title":"FEMS Microbiol Lett"},{"key":"2021041513065312300_b79","doi-asserted-by":"crossref","first-page":"6241","DOI":"10.1128\/AEM.71.10.6241-6246.2005","volume":"71","year":"2005","journal-title":"Appl Environ Microbiol"},{"key":"2021041513065312300_b80","first-page":"42","volume":"13","year":"1956","journal-title":"Microbiol Genet Bull"},{"key":"2021041513065312300_b81","doi-asserted-by":"crossref","first-page":"13386","DOI":"10.1073\/pnas.0504423102","volume":"102","year":"2005","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021041513065312300_b82","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1080\/09583150500187108","volume":"15","year":"2005","journal-title":"Biocontrol Sci Technol"},{"key":"2021041513065312300_b83","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1006\/fgbi.2001.1263","volume":"32","year":"2001","journal-title":"Fungal Genet Biol"},{"key":"2021041513065312300_b84","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1046\/j.1364-3703.2002.00144.x","volume":"3","year":"2002","journal-title":"Mol Plant Pathol"},{"key":"2021041513065312300_b85","first-page":"473","volume":"81","year":"1996","journal-title":"J Ferment Bioeng"},{"key":"2021041513065312300_b86","doi-asserted-by":"crossref","first-page":"1061","DOI":"10.1128\/AEM.65.3.1061-1070.1999","volume":"65","year":"1999","journal-title":"Appl Environ Microbiol"},{"key":"2021041513065312300_b87","doi-asserted-by":"crossref","first-page":"863","DOI":"10.1016\/S0981-9428(00)01198-0","volume":"38","year":"2000","journal-title":"Plant Physiol Biochem"},{"key":"2021041513065312300_b88","doi-asserted-by":"crossref","first-page":"7343","DOI":"10.1128\/AEM.69.12.7343-7353.2003","volume":"69","year":"2003","journal-title":"Appl Environ Microbiol"},{"key":"2021041513065312300_b89","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1007\/s11103-005-8883-z","volume":"59","year":"2005","journal-title":"Plant Mol Biol"}],"container-title":["Plant Physiology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/plphys\/article-pdf\/145\/3\/875\/37071025\/plphys_v145_3_875.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/plphys\/article-pdf\/145\/3\/875\/37071025\/plphys_v145_3_875.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,8,23]],"date-time":"2021-08-23T22:27:30Z","timestamp":1629757650000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/plphys\/article\/145\/3\/875\/6107226"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2007,9,20]]},"references-count":89,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2007,9,20]]},"published-print":{"date-parts":[[2007,11,5]]}},"URL":"https:\/\/doi.org\/10.1104\/pp.107.103689","relation":{},"ISSN":["1532-2548"],"issn-type":[{"value":"1532-2548","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2007,11,1]]},"published":{"date-parts":[[2007,9,20]]}}}