Transcriptional reprogramming underpins enhanced plant growth promotion by the biocontrol fungus Trichoderma hamatum GD12 during antagonistic interactions with Sclerotinia sclerotiorum in soil
Summary The free‐living soil fungus Trichoderma hamatum strain GD12 is notable amongst Trichoderma strains in both controlling plant diseases and stimulating plant growth, a property enhanced during its antagonistic interactions with pathogens in soil. These attributes, alongside its markedly expand...
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creator | Shaw, Sophie Le Cocq, Kate Paszkiewicz, Konrad Moore, Karen Winsbury, Rebecca de Torres Zabala, Marta Studholme, David J. Salmon, Deborah Thornton, Christopher R. Grant, Murray R. |
description | Summary
The free‐living soil fungus Trichoderma hamatum strain GD12 is notable amongst Trichoderma strains in both controlling plant diseases and stimulating plant growth, a property enhanced during its antagonistic interactions with pathogens in soil. These attributes, alongside its markedly expanded genome and proteome compared with other biocontrol and plant growth‐promoting Trichoderma strains, imply a rich potential for sustainable alternatives to synthetic pesticides and fertilizers for the control of plant disease and for increasing yields. The purpose of this study was to investigate the transcriptional responses of GD12 underpinning its biocontrol and plant growth promotion capabilities during antagonistic interactions with the pathogen Sclerotinia sclerotiorum in soil. Using an extensive mRNA‐seq study capturing different time points during the pathogen–antagonist interaction in soil, we show that dynamic and biphasic signatures in the GD12 transcriptome underpin its biocontrol and plant (lettuce) growth‐promoting activities. Functional predictions of differentially expressed genes demonstrate the enrichment of transcripts encoding proteins involved in transportation and oxidation–reduction reactions during both processes and an over‐representation of siderophores. We identify a biphasic response during biocontrol characterized by a significant induction of transcripts encoding small‐secreted cysteine‐rich proteins, secondary metabolite‐producing gene clusters and genes unique to GD12. These data support the hypothesis that Sclerotinia biocontrol is mediated by the synthesis and secretion of antifungal compounds and that GD12's unique reservoir of uncharacterized genes is actively recruited during the effective biological control of a plurivorous plant pathogen. |
doi_str_mv | 10.1111/mpp.12429 |
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The free‐living soil fungus Trichoderma hamatum strain GD12 is notable amongst Trichoderma strains in both controlling plant diseases and stimulating plant growth, a property enhanced during its antagonistic interactions with pathogens in soil. These attributes, alongside its markedly expanded genome and proteome compared with other biocontrol and plant growth‐promoting Trichoderma strains, imply a rich potential for sustainable alternatives to synthetic pesticides and fertilizers for the control of plant disease and for increasing yields. The purpose of this study was to investigate the transcriptional responses of GD12 underpinning its biocontrol and plant growth promotion capabilities during antagonistic interactions with the pathogen Sclerotinia sclerotiorum in soil. Using an extensive mRNA‐seq study capturing different time points during the pathogen–antagonist interaction in soil, we show that dynamic and biphasic signatures in the GD12 transcriptome underpin its biocontrol and plant (lettuce) growth‐promoting activities. Functional predictions of differentially expressed genes demonstrate the enrichment of transcripts encoding proteins involved in transportation and oxidation–reduction reactions during both processes and an over‐representation of siderophores. We identify a biphasic response during biocontrol characterized by a significant induction of transcripts encoding small‐secreted cysteine‐rich proteins, secondary metabolite‐producing gene clusters and genes unique to GD12. These data support the hypothesis that Sclerotinia biocontrol is mediated by the synthesis and secretion of antifungal compounds and that GD12's unique reservoir of uncharacterized genes is actively recruited during the effective biological control of a plurivorous plant pathogen.</description><identifier>ISSN: 1464-6722</identifier><identifier>EISSN: 1364-3703</identifier><identifier>DOI: 10.1111/mpp.12429</identifier><identifier>PMID: 27187266</identifier><identifier>CODEN: MPPAFD</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Ascomycota - physiology ; biocontrol ; Cluster Analysis ; Gene Expression Profiling ; Gene Expression Regulation, Fungal ; Lactuca - growth & development ; Lactuca - microbiology ; Original ; Pathogens ; Pest Control, Biological ; Plant growth ; plant growth promotion ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; RNA-seq ; Sclerotinia ; Sclerotinia sclerotiorum ; Secondary Metabolism - genetics ; Sequence Analysis, RNA ; Soil ; Soil Microbiology ; Species Specificity ; Time Factors ; Transcription, Genetic ; Trichoderma - genetics ; Trichoderma hamatum ; Up-Regulation - genetics</subject><ispartof>Molecular plant pathology, 2016-12, Vol.17 (9), p.1425-1441</ispartof><rights>2016 The Authors. published by British Society for Plant Pathology and John Wiley & Sons Ltd</rights><rights>2016 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd.</rights><rights>2016 BSPP and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5549-59f087e6bdcdb533f2928b23d7cd0d0ee054bf3c94f290db10ec2823a1a88c83</citedby><cites>FETCH-LOGICAL-c5549-59f087e6bdcdb533f2928b23d7cd0d0ee054bf3c94f290db10ec2823a1a88c83</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6638342/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6638342/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,725,778,782,883,1414,11545,27907,27908,45557,45558,46035,46459,53774,53776</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27187266$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Shaw, Sophie</creatorcontrib><creatorcontrib>Le Cocq, Kate</creatorcontrib><creatorcontrib>Paszkiewicz, Konrad</creatorcontrib><creatorcontrib>Moore, Karen</creatorcontrib><creatorcontrib>Winsbury, Rebecca</creatorcontrib><creatorcontrib>de Torres Zabala, Marta</creatorcontrib><creatorcontrib>Studholme, David J.</creatorcontrib><creatorcontrib>Salmon, Deborah</creatorcontrib><creatorcontrib>Thornton, Christopher R.</creatorcontrib><creatorcontrib>Grant, Murray R.</creatorcontrib><title>Transcriptional reprogramming underpins enhanced plant growth promotion by the biocontrol fungus Trichoderma hamatum GD12 during antagonistic interactions with Sclerotinia sclerotiorum in soil</title><title>Molecular plant pathology</title><addtitle>Molecular Plant Pathology</addtitle><description>Summary
The free‐living soil fungus Trichoderma hamatum strain GD12 is notable amongst Trichoderma strains in both controlling plant diseases and stimulating plant growth, a property enhanced during its antagonistic interactions with pathogens in soil. These attributes, alongside its markedly expanded genome and proteome compared with other biocontrol and plant growth‐promoting Trichoderma strains, imply a rich potential for sustainable alternatives to synthetic pesticides and fertilizers for the control of plant disease and for increasing yields. The purpose of this study was to investigate the transcriptional responses of GD12 underpinning its biocontrol and plant growth promotion capabilities during antagonistic interactions with the pathogen Sclerotinia sclerotiorum in soil. Using an extensive mRNA‐seq study capturing different time points during the pathogen–antagonist interaction in soil, we show that dynamic and biphasic signatures in the GD12 transcriptome underpin its biocontrol and plant (lettuce) growth‐promoting activities. Functional predictions of differentially expressed genes demonstrate the enrichment of transcripts encoding proteins involved in transportation and oxidation–reduction reactions during both processes and an over‐representation of siderophores. We identify a biphasic response during biocontrol characterized by a significant induction of transcripts encoding small‐secreted cysteine‐rich proteins, secondary metabolite‐producing gene clusters and genes unique to GD12. These data support the hypothesis that Sclerotinia biocontrol is mediated by the synthesis and secretion of antifungal compounds and that GD12's unique reservoir of uncharacterized genes is actively recruited during the effective biological control of a plurivorous plant pathogen.</description><subject>Ascomycota - physiology</subject><subject>biocontrol</subject><subject>Cluster Analysis</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Fungal</subject><subject>Lactuca - growth & development</subject><subject>Lactuca - microbiology</subject><subject>Original</subject><subject>Pathogens</subject><subject>Pest Control, Biological</subject><subject>Plant growth</subject><subject>plant growth promotion</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>RNA-seq</subject><subject>Sclerotinia</subject><subject>Sclerotinia sclerotiorum</subject><subject>Secondary Metabolism - genetics</subject><subject>Sequence Analysis, RNA</subject><subject>Soil</subject><subject>Soil Microbiology</subject><subject>Species Specificity</subject><subject>Time Factors</subject><subject>Transcription, Genetic</subject><subject>Trichoderma - genetics</subject><subject>Trichoderma hamatum</subject><subject>Up-Regulation - genetics</subject><issn>1464-6722</issn><issn>1364-3703</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp1ks2O0zAQgCMEYn_gwAsgS1zYQ3f9l9i5IKEFCmKBSlupR8txnMRLbAc7ofTteDQc2q0ACV88kr_5ZmxPlj1D8BKldWWH4RJhissH2SkiBV0QBsnDFNMUFwzjk-wsxjsIEStx_jg7wQxxhoviNPu5DtJFFcwwGu9kD4Iegm-DtNa4Fkyu1mEwLgLtOumUrsHQSzeCNvjt2IHEWj9ngmoHxk6Dynjl3Rh8D5rJtVME62BU55PGStBJK8fJguUbhEE9hblEssnWOxNHo4Bxow5SzcYItiZVuFW9DqmEMxLEQ-xDchgHojf9k-xRI_uonx7282z97u36-v3i5svyw_Xrm4XKc1ou8rKBnOmiqlVd5YQ0uMS8wqRmqoY11BrmtGqIKmk6gXWFoFaYYyKR5Fxxcp692muHqbK6VjrdUfZiCMbKsBNeGvH3iTOdaP13URSEE4qT4OVBEPy3ScdRWBOV7tNraj9FgXgOGaOIkIS--Ae981NInzNTNKcEoXymLvaUCj7GoJtjMwiKeSxEGgvxeywS-_zP7o_k_Rwk4GoPbE2vd_83iU-r1b1ysc9IH6d_HDNk-CoKRlguNp-X4pZv4GpDPwpMfgG4JNiV</recordid><startdate>201612</startdate><enddate>201612</enddate><creator>Shaw, Sophie</creator><creator>Le Cocq, Kate</creator><creator>Paszkiewicz, Konrad</creator><creator>Moore, Karen</creator><creator>Winsbury, Rebecca</creator><creator>de Torres Zabala, Marta</creator><creator>Studholme, David J.</creator><creator>Salmon, Deborah</creator><creator>Thornton, Christopher R.</creator><creator>Grant, Murray R.</creator><general>Blackwell Publishing Ltd</general><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>BSCLL</scope><scope>24P</scope><scope>WIN</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>7QL</scope><scope>7QO</scope><scope>7T7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>5PM</scope></search><sort><creationdate>201612</creationdate><title>Transcriptional reprogramming underpins enhanced plant growth promotion by the biocontrol fungus Trichoderma hamatum GD12 during antagonistic interactions with Sclerotinia sclerotiorum in soil</title><author>Shaw, Sophie ; Le Cocq, Kate ; Paszkiewicz, Konrad ; Moore, Karen ; Winsbury, Rebecca ; de Torres Zabala, Marta ; Studholme, David J. ; Salmon, Deborah ; Thornton, Christopher R. ; Grant, Murray R.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5549-59f087e6bdcdb533f2928b23d7cd0d0ee054bf3c94f290db10ec2823a1a88c83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Ascomycota - physiology</topic><topic>biocontrol</topic><topic>Cluster Analysis</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Fungal</topic><topic>Lactuca - growth & development</topic><topic>Lactuca - microbiology</topic><topic>Original</topic><topic>Pathogens</topic><topic>Pest Control, Biological</topic><topic>Plant growth</topic><topic>plant growth promotion</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>RNA-seq</topic><topic>Sclerotinia</topic><topic>Sclerotinia sclerotiorum</topic><topic>Secondary Metabolism - genetics</topic><topic>Sequence Analysis, RNA</topic><topic>Soil</topic><topic>Soil Microbiology</topic><topic>Species Specificity</topic><topic>Time Factors</topic><topic>Transcription, Genetic</topic><topic>Trichoderma - genetics</topic><topic>Trichoderma hamatum</topic><topic>Up-Regulation - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Shaw, Sophie</creatorcontrib><creatorcontrib>Le Cocq, Kate</creatorcontrib><creatorcontrib>Paszkiewicz, Konrad</creatorcontrib><creatorcontrib>Moore, Karen</creatorcontrib><creatorcontrib>Winsbury, Rebecca</creatorcontrib><creatorcontrib>de Torres Zabala, Marta</creatorcontrib><creatorcontrib>Studholme, David J.</creatorcontrib><creatorcontrib>Salmon, Deborah</creatorcontrib><creatorcontrib>Thornton, Christopher R.</creatorcontrib><creatorcontrib>Grant, Murray R.</creatorcontrib><collection>Istex</collection><collection>Wiley-Blackwell Open Access Titles</collection><collection>Wiley Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular plant pathology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shaw, Sophie</au><au>Le Cocq, Kate</au><au>Paszkiewicz, Konrad</au><au>Moore, Karen</au><au>Winsbury, Rebecca</au><au>de Torres Zabala, Marta</au><au>Studholme, David J.</au><au>Salmon, Deborah</au><au>Thornton, Christopher R.</au><au>Grant, Murray R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Transcriptional reprogramming underpins enhanced plant growth promotion by the biocontrol fungus Trichoderma hamatum GD12 during antagonistic interactions with Sclerotinia sclerotiorum in soil</atitle><jtitle>Molecular plant pathology</jtitle><addtitle>Molecular Plant Pathology</addtitle><date>2016-12</date><risdate>2016</risdate><volume>17</volume><issue>9</issue><spage>1425</spage><epage>1441</epage><pages>1425-1441</pages><issn>1464-6722</issn><eissn>1364-3703</eissn><coden>MPPAFD</coden><abstract>Summary
The free‐living soil fungus Trichoderma hamatum strain GD12 is notable amongst Trichoderma strains in both controlling plant diseases and stimulating plant growth, a property enhanced during its antagonistic interactions with pathogens in soil. These attributes, alongside its markedly expanded genome and proteome compared with other biocontrol and plant growth‐promoting Trichoderma strains, imply a rich potential for sustainable alternatives to synthetic pesticides and fertilizers for the control of plant disease and for increasing yields. The purpose of this study was to investigate the transcriptional responses of GD12 underpinning its biocontrol and plant growth promotion capabilities during antagonistic interactions with the pathogen Sclerotinia sclerotiorum in soil. Using an extensive mRNA‐seq study capturing different time points during the pathogen–antagonist interaction in soil, we show that dynamic and biphasic signatures in the GD12 transcriptome underpin its biocontrol and plant (lettuce) growth‐promoting activities. Functional predictions of differentially expressed genes demonstrate the enrichment of transcripts encoding proteins involved in transportation and oxidation–reduction reactions during both processes and an over‐representation of siderophores. We identify a biphasic response during biocontrol characterized by a significant induction of transcripts encoding small‐secreted cysteine‐rich proteins, secondary metabolite‐producing gene clusters and genes unique to GD12. These data support the hypothesis that Sclerotinia biocontrol is mediated by the synthesis and secretion of antifungal compounds and that GD12's unique reservoir of uncharacterized genes is actively recruited during the effective biological control of a plurivorous plant pathogen.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>27187266</pmid><doi>10.1111/mpp.12429</doi><tpages>17</tpages><oa>free_for_read</oa></addata></record> |
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source | MEDLINE; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Wiley-Blackwell Open Access Titles; PubMed Central |
subjects | Ascomycota - physiology biocontrol Cluster Analysis Gene Expression Profiling Gene Expression Regulation, Fungal Lactuca - growth & development Lactuca - microbiology Original Pathogens Pest Control, Biological Plant growth plant growth promotion RNA, Messenger - genetics RNA, Messenger - metabolism RNA-seq Sclerotinia Sclerotinia sclerotiorum Secondary Metabolism - genetics Sequence Analysis, RNA Soil Soil Microbiology Species Specificity Time Factors Transcription, Genetic Trichoderma - genetics Trichoderma hamatum Up-Regulation - genetics |
title | Transcriptional reprogramming underpins enhanced plant growth promotion by the biocontrol fungus Trichoderma hamatum GD12 during antagonistic interactions with Sclerotinia sclerotiorum in soil |
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