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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Veröffentlicht in:Molecular plant pathology 2016-12, Vol.17 (9), p.1425-1441
Hauptverfasser: 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.
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container_end_page 1441
container_issue 9
container_start_page 1425
container_title Molecular plant pathology
container_volume 17
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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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. 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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. 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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. 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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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