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B-3 Ethylene Response Factor MtERF1-1 Mediates Resistance to a Subset of Root Pathogens in Medicago truncatula without Adversely Affecting Symbiosis with Rhizobia
The fungal necrotrophic pathogen Rhizoctonia solani is a significant constraint to a range of crops as diverse as cereals, canola, and legumes. Despite wide-ranging germplasm screens in many of these crops, no strong genetic resistance has been identified, suggesting that alternative strategies to i...
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Published in: | Plant physiology (Bethesda) 2010-10, Vol.154 (2), p.861-873 |
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description | The fungal necrotrophic pathogen Rhizoctonia solani is a significant constraint to a range of crops as diverse as cereals, canola, and legumes. Despite wide-ranging germplasm screens in many of these crops, no strong genetic resistance has been identified, suggesting that alternative strategies to improve resistance are required. In this study, we characterize moderate resistance to R. solani anastomosis group 8 identified in Medicago truncatula. The activity of the ethylene- and jasmonate-responsive GCC box promoter element was associated with moderate resistance, as was the induction of the B-3 subgroup of ethylene response transcription factors (ERFs). Genes of the B-1 subgroup showed no significant response to R. solani infection. Overexpression of a B-3 ERF, MtERF1-1, in Medicago roots increased resistance to R. solani as well as an oomycete root pathogen, Phytophthora medicaginis, but not root knot nematode. These results indicate that targeting specific regulators of ethylene defense may enhance resistance to an important subset of root pathogens. We also demonstrate that overexpression of MtERF1-1 enhances disease resistance without apparent impact on nodulation in the A17 background, while overexpression in sickle reduced the hypernodulation phenotype. This suggests that under normal regulation of nodulation, enhanced resistance to root diseases can be uncoupled from symbiotic plant-microbe interactions in the same tissue and that ethylene/ERF regulation of nodule number is distinct from the defenses regulated by B-3 ERFs. Furthermore, unlike the stunted phenotype previously described for Arabidopsis (Arabidopsis thaliana) ubiquitously overexpressing B-3 ERFs, overexpression of MtERF1-1 in M. truncatula roots did not show adverse effects on plant development. |
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Despite wide-ranging germplasm screens in many of these crops, no strong genetic resistance has been identified, suggesting that alternative strategies to improve resistance are required. In this study, we characterize moderate resistance to R. solani anastomosis group 8 identified in Medicago truncatula. The activity of the ethylene- and jasmonate-responsive GCC box promoter element was associated with moderate resistance, as was the induction of the B-3 subgroup of ethylene response transcription factors (ERFs). Genes of the B-1 subgroup showed no significant response to R. solani infection. Overexpression of a B-3 ERF, MtERF1-1, in Medicago roots increased resistance to R. solani as well as an oomycete root pathogen, Phytophthora medicaginis, but not root knot nematode. These results indicate that targeting specific regulators of ethylene defense may enhance resistance to an important subset of root pathogens. We also demonstrate that overexpression of MtERF1-1 enhances disease resistance without apparent impact on nodulation in the A17 background, while overexpression in sickle reduced the hypernodulation phenotype. This suggests that under normal regulation of nodulation, enhanced resistance to root diseases can be uncoupled from symbiotic plant-microbe interactions in the same tissue and that ethylene/ERF regulation of nodule number is distinct from the defenses regulated by B-3 ERFs. Furthermore, unlike the stunted phenotype previously described for Arabidopsis (Arabidopsis thaliana) ubiquitously overexpressing B-3 ERFs, overexpression of MtERF1-1 in M. truncatula roots did not show adverse effects on plant development.</description><identifier>ISSN: 0032-0889</identifier><identifier>ISSN: 1532-2548</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.110.163949</identifier><identifier>PMID: 20713618</identifier><identifier>CODEN: PPHYA5</identifier><language>eng</language><publisher>Rockville, MD: American Society of Plant Biologists</publisher><subject>Arabidopsis thaliana ; Bacteria ; Biological and medical sciences ; Disease resistance ; Ethylenes - pharmacology ; Fundamental and applied biological sciences. Psychology ; Gene Expression Regulation, Plant ; Infections ; Inoculation ; Leaves ; Medicago ; Medicago truncatula ; Medicago truncatula - genetics ; Medicago truncatula - growth & development ; Medicago truncatula - immunology ; Medicago truncatula - microbiology ; Nematoda ; Oomycetes ; Pathogens ; Phytopathology. Animal pests. Plant and forest protection ; Phytophthora medicaginis ; Plant diseases ; Plant Immunity ; Plant physiology and development ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant Root Nodulation ; Plant roots ; Plant Roots - microbiology ; Plants ; PLANTS INTERACTING WITH OTHER ORGANISMS ; Plants, Genetically Modified - genetics ; Plants, Genetically Modified - growth & development ; Plants, Genetically Modified - immunology ; Plants, Genetically Modified - microbiology ; Promoter Regions, Genetic ; Rhizoctonia - pathogenicity ; Rhizoctonia solani ; RNA, Plant - genetics ; Seedlings ; Sinorhizobium meliloti - physiology ; Skis ; Symbiosis ; Transcription Factors - genetics ; Transcription Factors - metabolism</subject><ispartof>Plant physiology (Bethesda), 2010-10, Vol.154 (2), p.861-873</ispartof><rights>2010 American Society of Plant Biologists</rights><rights>2015 INIST-CNRS</rights><rights>2010 American Society of Plant Biologists 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c455t-74334347d32f60c1a4eff481459a48991882203ca927266c77937899dcf91a313</citedby><cites>FETCH-LOGICAL-c455t-74334347d32f60c1a4eff481459a48991882203ca927266c77937899dcf91a313</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/20779838$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/20779838$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=23296929$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20713618$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Anderson, Jonathan P</creatorcontrib><creatorcontrib>Lichtenzveig, Judith</creatorcontrib><creatorcontrib>Gleason, Cynthia</creatorcontrib><creatorcontrib>Oliver, Richard P</creatorcontrib><creatorcontrib>Singh, Karam B</creatorcontrib><title>B-3 Ethylene Response Factor MtERF1-1 Mediates Resistance to a Subset of Root Pathogens in Medicago truncatula without Adversely Affecting Symbiosis with Rhizobia</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>The fungal necrotrophic pathogen Rhizoctonia solani is a significant constraint to a range of crops as diverse as cereals, canola, and legumes. Despite wide-ranging germplasm screens in many of these crops, no strong genetic resistance has been identified, suggesting that alternative strategies to improve resistance are required. In this study, we characterize moderate resistance to R. solani anastomosis group 8 identified in Medicago truncatula. The activity of the ethylene- and jasmonate-responsive GCC box promoter element was associated with moderate resistance, as was the induction of the B-3 subgroup of ethylene response transcription factors (ERFs). Genes of the B-1 subgroup showed no significant response to R. solani infection. Overexpression of a B-3 ERF, MtERF1-1, in Medicago roots increased resistance to R. solani as well as an oomycete root pathogen, Phytophthora medicaginis, but not root knot nematode. These results indicate that targeting specific regulators of ethylene defense may enhance resistance to an important subset of root pathogens. We also demonstrate that overexpression of MtERF1-1 enhances disease resistance without apparent impact on nodulation in the A17 background, while overexpression in sickle reduced the hypernodulation phenotype. This suggests that under normal regulation of nodulation, enhanced resistance to root diseases can be uncoupled from symbiotic plant-microbe interactions in the same tissue and that ethylene/ERF regulation of nodule number is distinct from the defenses regulated by B-3 ERFs. Furthermore, unlike the stunted phenotype previously described for Arabidopsis (Arabidopsis thaliana) ubiquitously overexpressing B-3 ERFs, overexpression of MtERF1-1 in M. truncatula roots did not show adverse effects on plant development.</description><subject>Arabidopsis thaliana</subject><subject>Bacteria</subject><subject>Biological and medical sciences</subject><subject>Disease resistance</subject><subject>Ethylenes - pharmacology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Expression Regulation, Plant</subject><subject>Infections</subject><subject>Inoculation</subject><subject>Leaves</subject><subject>Medicago</subject><subject>Medicago truncatula</subject><subject>Medicago truncatula - genetics</subject><subject>Medicago truncatula - growth & development</subject><subject>Medicago truncatula - immunology</subject><subject>Medicago truncatula - microbiology</subject><subject>Nematoda</subject><subject>Oomycetes</subject><subject>Pathogens</subject><subject>Phytopathology. Animal pests. Plant and forest protection</subject><subject>Phytophthora medicaginis</subject><subject>Plant diseases</subject><subject>Plant Immunity</subject><subject>Plant physiology and development</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Root Nodulation</subject><subject>Plant roots</subject><subject>Plant Roots - microbiology</subject><subject>Plants</subject><subject>PLANTS INTERACTING WITH OTHER ORGANISMS</subject><subject>Plants, Genetically Modified - genetics</subject><subject>Plants, Genetically Modified - growth & development</subject><subject>Plants, Genetically Modified - immunology</subject><subject>Plants, Genetically Modified - microbiology</subject><subject>Promoter Regions, Genetic</subject><subject>Rhizoctonia - pathogenicity</subject><subject>Rhizoctonia solani</subject><subject>RNA, Plant - genetics</subject><subject>Seedlings</subject><subject>Sinorhizobium meliloti - physiology</subject><subject>Skis</subject><subject>Symbiosis</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><issn>0032-0889</issn><issn>1532-2548</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><recordid>eNp9kk-PEyEYxonRuLV69KhyMZ5m5d_MwMWkblo12Y2mdc-EUmjZTIdZYNbUj-MnlenUdb14egnvj-cB3geAlxidY4zY-64b6jmuqGDiEZjgkpKClIw_BhOE8hpxLs7AsxhvEEKYYvYUnBFUY1phPgG_PhYUztPu0JjWwKWJnW-jgQulkw_wKs2XC1xgeGU2TiUTB8LFpFptYPJQwVW_jiZBb-HS-wS_qbTzW9NG6NrjIa22HqbQt1qlvlHwh8tAn-Bsc2dCNM0Bzqw1Orl2C1eH_dr5rH-k4HLnfvq1U8_BE6uaaF6c6hRcL-bfLz4Xl18_fbmYXRaalWUqakYpo6zeUGIrpLFixlrGMSuFYlwIzDkhiGolSE2qSte1oHXe32grsKKYTsGHUbfr13uz0aZNQTWyC26vwkF65eS_ndbt5NbfSZJ_HmX3KXh3Egj-tjcxyb2L2jSNao3vo-Q1wUSIo9X_ybqsqooLIjJZjKQOPsZg7P19MJJDAGTXDVWOAcj864ePuKf_TDwDb0-Ailo1NuRZuviXo0RUo_GrkbuJOQkPdWrB6aDzZuxb5aXahqxxvSI5YAhzwbMG_Q3r3sxl</recordid><startdate>20101001</startdate><enddate>20101001</enddate><creator>Anderson, Jonathan P</creator><creator>Lichtenzveig, Judith</creator><creator>Gleason, Cynthia</creator><creator>Oliver, Richard P</creator><creator>Singh, Karam B</creator><general>American Society of Plant Biologists</general><scope>FBQ</scope><scope>IQODW</scope><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>7X8</scope><scope>7QL</scope><scope>C1K</scope><scope>5PM</scope></search><sort><creationdate>20101001</creationdate><title>B-3 Ethylene Response Factor MtERF1-1 Mediates Resistance to a Subset of Root Pathogens in Medicago truncatula without Adversely Affecting Symbiosis with Rhizobia</title><author>Anderson, Jonathan P ; Lichtenzveig, Judith ; Gleason, Cynthia ; Oliver, Richard P ; Singh, Karam B</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c455t-74334347d32f60c1a4eff481459a48991882203ca927266c77937899dcf91a313</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Arabidopsis thaliana</topic><topic>Bacteria</topic><topic>Biological and medical sciences</topic><topic>Disease resistance</topic><topic>Ethylenes - pharmacology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Expression Regulation, Plant</topic><topic>Infections</topic><topic>Inoculation</topic><topic>Leaves</topic><topic>Medicago</topic><topic>Medicago truncatula</topic><topic>Medicago truncatula - genetics</topic><topic>Medicago truncatula - growth & development</topic><topic>Medicago truncatula - immunology</topic><topic>Medicago truncatula - microbiology</topic><topic>Nematoda</topic><topic>Oomycetes</topic><topic>Pathogens</topic><topic>Phytopathology. Animal pests. Plant and forest protection</topic><topic>Phytophthora medicaginis</topic><topic>Plant diseases</topic><topic>Plant Immunity</topic><topic>Plant physiology and development</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plant Root Nodulation</topic><topic>Plant roots</topic><topic>Plant Roots - microbiology</topic><topic>Plants</topic><topic>PLANTS INTERACTING WITH OTHER ORGANISMS</topic><topic>Plants, Genetically Modified - genetics</topic><topic>Plants, Genetically Modified - growth & development</topic><topic>Plants, Genetically Modified - immunology</topic><topic>Plants, Genetically Modified - microbiology</topic><topic>Promoter Regions, Genetic</topic><topic>Rhizoctonia - pathogenicity</topic><topic>Rhizoctonia solani</topic><topic>RNA, Plant - genetics</topic><topic>Seedlings</topic><topic>Sinorhizobium meliloti - physiology</topic><topic>Skis</topic><topic>Symbiosis</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Anderson, Jonathan P</creatorcontrib><creatorcontrib>Lichtenzveig, Judith</creatorcontrib><creatorcontrib>Gleason, Cynthia</creatorcontrib><creatorcontrib>Oliver, Richard P</creatorcontrib><creatorcontrib>Singh, Karam B</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environmental Sciences and Pollution Management</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Anderson, Jonathan P</au><au>Lichtenzveig, Judith</au><au>Gleason, Cynthia</au><au>Oliver, Richard P</au><au>Singh, Karam B</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>B-3 Ethylene Response Factor MtERF1-1 Mediates Resistance to a Subset of Root Pathogens in Medicago truncatula without Adversely Affecting Symbiosis with Rhizobia</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2010-10-01</date><risdate>2010</risdate><volume>154</volume><issue>2</issue><spage>861</spage><epage>873</epage><pages>861-873</pages><issn>0032-0889</issn><issn>1532-2548</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>The fungal necrotrophic pathogen Rhizoctonia solani is a significant constraint to a range of crops as diverse as cereals, canola, and legumes. Despite wide-ranging germplasm screens in many of these crops, no strong genetic resistance has been identified, suggesting that alternative strategies to improve resistance are required. In this study, we characterize moderate resistance to R. solani anastomosis group 8 identified in Medicago truncatula. The activity of the ethylene- and jasmonate-responsive GCC box promoter element was associated with moderate resistance, as was the induction of the B-3 subgroup of ethylene response transcription factors (ERFs). Genes of the B-1 subgroup showed no significant response to R. solani infection. Overexpression of a B-3 ERF, MtERF1-1, in Medicago roots increased resistance to R. solani as well as an oomycete root pathogen, Phytophthora medicaginis, but not root knot nematode. These results indicate that targeting specific regulators of ethylene defense may enhance resistance to an important subset of root pathogens. We also demonstrate that overexpression of MtERF1-1 enhances disease resistance without apparent impact on nodulation in the A17 background, while overexpression in sickle reduced the hypernodulation phenotype. This suggests that under normal regulation of nodulation, enhanced resistance to root diseases can be uncoupled from symbiotic plant-microbe interactions in the same tissue and that ethylene/ERF regulation of nodule number is distinct from the defenses regulated by B-3 ERFs. Furthermore, unlike the stunted phenotype previously described for Arabidopsis (Arabidopsis thaliana) ubiquitously overexpressing B-3 ERFs, overexpression of MtERF1-1 in M. truncatula roots did not show adverse effects on plant development.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>20713618</pmid><doi>10.1104/pp.110.163949</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis thaliana Bacteria Biological and medical sciences Disease resistance Ethylenes - pharmacology Fundamental and applied biological sciences. Psychology Gene Expression Regulation, Plant Infections Inoculation Leaves Medicago Medicago truncatula Medicago truncatula - genetics Medicago truncatula - growth & development Medicago truncatula - immunology Medicago truncatula - microbiology Nematoda Oomycetes Pathogens Phytopathology. Animal pests. Plant and forest protection Phytophthora medicaginis Plant diseases Plant Immunity Plant physiology and development Plant Proteins - genetics Plant Proteins - metabolism Plant Root Nodulation Plant roots Plant Roots - microbiology Plants PLANTS INTERACTING WITH OTHER ORGANISMS Plants, Genetically Modified - genetics Plants, Genetically Modified - growth & development Plants, Genetically Modified - immunology Plants, Genetically Modified - microbiology Promoter Regions, Genetic Rhizoctonia - pathogenicity Rhizoctonia solani RNA, Plant - genetics Seedlings Sinorhizobium meliloti - physiology Skis Symbiosis Transcription Factors - genetics Transcription Factors - metabolism |
title | B-3 Ethylene Response Factor MtERF1-1 Mediates Resistance to a Subset of Root Pathogens in Medicago truncatula without Adversely Affecting Symbiosis with Rhizobia |
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