Double-Wing Motif Protein is a Novel Biofilm Regulatory Factor of the Plant Disease Biocontrol Agent, Bacillus subtilis
Transposon mutagenesis screening of Bacillus subtilis YB-1471, a novel rhizosphere biocontrol agent of Fusarium crown rot (FCR) of wheat, resulted in the identification of orf04391, linked to reduced biofilm formation. The gene encodes a protein possessing a putative tertiary structure of a “double-...
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| Veröffentlicht in: | Journal of agricultural and food chemistry 2024-09, Vol.72 (37), p.20273-20285 |
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| container_title | Journal of agricultural and food chemistry |
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| creator | Dong, Qianqian Chang, Yinghang Goodwin, Paul H. Liu, Qingxiang Xu, Wen Xia, Mingcong Zhang, Jie Sun, Runhong Xu, Shuxia Wu, Chao Wu, Kun Yang, Lirong |
| description | Transposon mutagenesis screening of Bacillus subtilis YB-1471, a novel rhizosphere biocontrol agent of Fusarium crown rot (FCR) of wheat, resulted in the identification of orf04391, linked to reduced biofilm formation. The gene encodes a protein possessing a putative tertiary structure of a “double-wing” DNA-binding domain. Expression of orf04391 increased during biofilm development in stationary cultures and during rapid growth in shaking cultures. An orf04391 deletion strain showed reduced biofilm production related to lower levels of the extracellular matrix, and the mutant also had reduced sporulation, adhesion, root colonization, and FCR biocontrol efficiency. Transcriptome analysis of YB-1471 and Δorf04391 in stationary culture showed that the loss of orf04391 resulted in altered expression of numerous genes, including sinI, an initiator of biofilm formation. DNA binding was shown with his-tagged Orf04391 binding to the sinIR operon in vivo and in vitro. Orf04391 appears to be a transcriptional regulator of biofilm formation in B. subtilis through the Spo0A-SinI/SinR pathway. |
| doi_str_mv | 10.1021/acs.jafc.4c02192 |
| format | Article |
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The gene encodes a protein possessing a putative tertiary structure of a “double-wing” DNA-binding domain. Expression of orf04391 increased during biofilm development in stationary cultures and during rapid growth in shaking cultures. An orf04391 deletion strain showed reduced biofilm production related to lower levels of the extracellular matrix, and the mutant also had reduced sporulation, adhesion, root colonization, and FCR biocontrol efficiency. Transcriptome analysis of YB-1471 and Δorf04391 in stationary culture showed that the loss of orf04391 resulted in altered expression of numerous genes, including sinI, an initiator of biofilm formation. DNA binding was shown with his-tagged Orf04391 binding to the sinIR operon in vivo and in vitro. Orf04391 appears to be a transcriptional regulator of biofilm formation in B. subtilis through the Spo0A-SinI/SinR pathway.</description><identifier>ISSN: 0021-8561</identifier><identifier>ISSN: 1520-5118</identifier><identifier>EISSN: 1520-5118</identifier><identifier>DOI: 10.1021/acs.jafc.4c02192</identifier><identifier>PMID: 39226040</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>adhesion ; Agricultural and Environmental Chemistry ; Bacillus subtilis ; Bacillus subtilis - genetics ; Bacillus subtilis - metabolism ; Bacterial Proteins - chemistry ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; biofilm ; Biofilms - growth & development ; biological control ; biological control agents ; crown rot ; DNA ; DNA-binding domains ; extracellular matrix ; food chemistry ; Fusarium ; Fusarium - genetics ; Fusarium - metabolism ; Fusarium - physiology ; Gene Expression Regulation, Bacterial ; mutagenesis ; mutants ; operon ; Plant Diseases - microbiology ; rhizosphere ; sporulation ; transcription factors ; transcriptomics ; transposons ; Triticum - microbiology ; wheat</subject><ispartof>Journal of agricultural and food chemistry, 2024-09, Vol.72 (37), p.20273-20285</ispartof><rights>2024 American Chemical Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-a252t-2808636a3294928c41e25138236b201ed03a6d4ae510b7c2f5ebb361904e2a5d3</cites><orcidid>0000-0003-4199-100X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://pubs.acs.org/doi/pdf/10.1021/acs.jafc.4c02192$$EPDF$$P50$$Gacs$$H</linktopdf><linktohtml>$$Uhttps://pubs.acs.org/doi/10.1021/acs.jafc.4c02192$$EHTML$$P50$$Gacs$$H</linktohtml><link.rule.ids>314,776,780,2752,27053,27901,27902,56713,56763</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39226040$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Dong, Qianqian</creatorcontrib><creatorcontrib>Chang, Yinghang</creatorcontrib><creatorcontrib>Goodwin, Paul H.</creatorcontrib><creatorcontrib>Liu, Qingxiang</creatorcontrib><creatorcontrib>Xu, Wen</creatorcontrib><creatorcontrib>Xia, Mingcong</creatorcontrib><creatorcontrib>Zhang, Jie</creatorcontrib><creatorcontrib>Sun, Runhong</creatorcontrib><creatorcontrib>Xu, Shuxia</creatorcontrib><creatorcontrib>Wu, Chao</creatorcontrib><creatorcontrib>Wu, Kun</creatorcontrib><creatorcontrib>Yang, Lirong</creatorcontrib><title>Double-Wing Motif Protein is a Novel Biofilm Regulatory Factor of the Plant Disease Biocontrol Agent, Bacillus subtilis</title><title>Journal of agricultural and food chemistry</title><addtitle>J. Agric. Food Chem</addtitle><description>Transposon mutagenesis screening of Bacillus subtilis YB-1471, a novel rhizosphere biocontrol agent of Fusarium crown rot (FCR) of wheat, resulted in the identification of orf04391, linked to reduced biofilm formation. The gene encodes a protein possessing a putative tertiary structure of a “double-wing” DNA-binding domain. Expression of orf04391 increased during biofilm development in stationary cultures and during rapid growth in shaking cultures. An orf04391 deletion strain showed reduced biofilm production related to lower levels of the extracellular matrix, and the mutant also had reduced sporulation, adhesion, root colonization, and FCR biocontrol efficiency. Transcriptome analysis of YB-1471 and Δorf04391 in stationary culture showed that the loss of orf04391 resulted in altered expression of numerous genes, including sinI, an initiator of biofilm formation. DNA binding was shown with his-tagged Orf04391 binding to the sinIR operon in vivo and in vitro. Orf04391 appears to be a transcriptional regulator of biofilm formation in B. subtilis through the Spo0A-SinI/SinR pathway.</description><subject>adhesion</subject><subject>Agricultural and Environmental Chemistry</subject><subject>Bacillus subtilis</subject><subject>Bacillus subtilis - genetics</subject><subject>Bacillus subtilis - metabolism</subject><subject>Bacterial Proteins - chemistry</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>biofilm</subject><subject>Biofilms - growth & development</subject><subject>biological control</subject><subject>biological control agents</subject><subject>crown rot</subject><subject>DNA</subject><subject>DNA-binding domains</subject><subject>extracellular matrix</subject><subject>food chemistry</subject><subject>Fusarium</subject><subject>Fusarium - genetics</subject><subject>Fusarium - metabolism</subject><subject>Fusarium - physiology</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>mutagenesis</subject><subject>mutants</subject><subject>operon</subject><subject>Plant Diseases - microbiology</subject><subject>rhizosphere</subject><subject>sporulation</subject><subject>transcription factors</subject><subject>transcriptomics</subject><subject>transposons</subject><subject>Triticum - microbiology</subject><subject>wheat</subject><issn>0021-8561</issn><issn>1520-5118</issn><issn>1520-5118</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkU1PGzEQhi1ERdLAnRPykQObju31fhwJKRSJL1Wtelx5ndlg5KxT29sq_74OCb0hcRqN9byvrHkIOWUwZcDZF6XD9EV1eprrtNb8gIyZ5JBJxqpDMob0mFWyYCPyOYQXAKhkCUdkJGrOC8hhTP7O3dBazH6ZfknvXTQdffIuoumpCVTRB_cHLZ0Z1xm7ot9xOVgVnd_Qa6XTpK6j8Rnpk1V9pHMTUAXc4tr10TtLL5fYxws6U9pYOwQahjYaa8Ix-dQpG_BkPyfk5_XXH1ffsrvHm9ury7tMccljxiuoClEoweu85pXOGXLJRMVF0XJguAChikWuUDJoS807iW0rClZDjlzJhZiQ813v2rvfA4bYrEzQaNN_0Q2hEUyKsmKsFh9A0z1LmYsyobBDtXcheOyatTcr5TcNg2Zrpklmmq2ZZm8mRc727UO7wsX_wJuKBFzsgNeoG3yf7vJ-3z9PypiF</recordid><startdate>20240918</startdate><enddate>20240918</enddate><creator>Dong, Qianqian</creator><creator>Chang, Yinghang</creator><creator>Goodwin, Paul H.</creator><creator>Liu, Qingxiang</creator><creator>Xu, Wen</creator><creator>Xia, Mingcong</creator><creator>Zhang, Jie</creator><creator>Sun, Runhong</creator><creator>Xu, Shuxia</creator><creator>Wu, Chao</creator><creator>Wu, Kun</creator><creator>Yang, Lirong</creator><general>American Chemical Society</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>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0003-4199-100X</orcidid></search><sort><creationdate>20240918</creationdate><title>Double-Wing Motif Protein is a Novel Biofilm Regulatory Factor of the Plant Disease Biocontrol Agent, Bacillus subtilis</title><author>Dong, Qianqian ; Chang, Yinghang ; Goodwin, Paul H. ; Liu, Qingxiang ; Xu, Wen ; Xia, Mingcong ; Zhang, Jie ; Sun, Runhong ; Xu, Shuxia ; Wu, Chao ; Wu, Kun ; Yang, Lirong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a252t-2808636a3294928c41e25138236b201ed03a6d4ae510b7c2f5ebb361904e2a5d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>adhesion</topic><topic>Agricultural and Environmental Chemistry</topic><topic>Bacillus subtilis</topic><topic>Bacillus subtilis - genetics</topic><topic>Bacillus subtilis - metabolism</topic><topic>Bacterial Proteins - chemistry</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>biofilm</topic><topic>Biofilms - growth & development</topic><topic>biological control</topic><topic>biological control agents</topic><topic>crown rot</topic><topic>DNA</topic><topic>DNA-binding domains</topic><topic>extracellular matrix</topic><topic>food chemistry</topic><topic>Fusarium</topic><topic>Fusarium - genetics</topic><topic>Fusarium - metabolism</topic><topic>Fusarium - physiology</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>mutagenesis</topic><topic>mutants</topic><topic>operon</topic><topic>Plant Diseases - microbiology</topic><topic>rhizosphere</topic><topic>sporulation</topic><topic>transcription factors</topic><topic>transcriptomics</topic><topic>transposons</topic><topic>Triticum - microbiology</topic><topic>wheat</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Dong, Qianqian</creatorcontrib><creatorcontrib>Chang, Yinghang</creatorcontrib><creatorcontrib>Goodwin, Paul H.</creatorcontrib><creatorcontrib>Liu, Qingxiang</creatorcontrib><creatorcontrib>Xu, Wen</creatorcontrib><creatorcontrib>Xia, Mingcong</creatorcontrib><creatorcontrib>Zhang, Jie</creatorcontrib><creatorcontrib>Sun, Runhong</creatorcontrib><creatorcontrib>Xu, Shuxia</creatorcontrib><creatorcontrib>Wu, Chao</creatorcontrib><creatorcontrib>Wu, Kun</creatorcontrib><creatorcontrib>Yang, Lirong</creatorcontrib><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>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Journal of agricultural and food chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dong, Qianqian</au><au>Chang, Yinghang</au><au>Goodwin, Paul H.</au><au>Liu, Qingxiang</au><au>Xu, Wen</au><au>Xia, Mingcong</au><au>Zhang, Jie</au><au>Sun, Runhong</au><au>Xu, Shuxia</au><au>Wu, Chao</au><au>Wu, Kun</au><au>Yang, Lirong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Double-Wing Motif Protein is a Novel Biofilm Regulatory Factor of the Plant Disease Biocontrol Agent, Bacillus subtilis</atitle><jtitle>Journal of agricultural and food chemistry</jtitle><addtitle>J. Agric. Food Chem</addtitle><date>2024-09-18</date><risdate>2024</risdate><volume>72</volume><issue>37</issue><spage>20273</spage><epage>20285</epage><pages>20273-20285</pages><issn>0021-8561</issn><issn>1520-5118</issn><eissn>1520-5118</eissn><abstract>Transposon mutagenesis screening of Bacillus subtilis YB-1471, a novel rhizosphere biocontrol agent of Fusarium crown rot (FCR) of wheat, resulted in the identification of orf04391, linked to reduced biofilm formation. The gene encodes a protein possessing a putative tertiary structure of a “double-wing” DNA-binding domain. Expression of orf04391 increased during biofilm development in stationary cultures and during rapid growth in shaking cultures. An orf04391 deletion strain showed reduced biofilm production related to lower levels of the extracellular matrix, and the mutant also had reduced sporulation, adhesion, root colonization, and FCR biocontrol efficiency. Transcriptome analysis of YB-1471 and Δorf04391 in stationary culture showed that the loss of orf04391 resulted in altered expression of numerous genes, including sinI, an initiator of biofilm formation. DNA binding was shown with his-tagged Orf04391 binding to the sinIR operon in vivo and in vitro. Orf04391 appears to be a transcriptional regulator of biofilm formation in B. subtilis through the Spo0A-SinI/SinR pathway.</abstract><cop>United States</cop><pub>American Chemical Society</pub><pmid>39226040</pmid><doi>10.1021/acs.jafc.4c02192</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-4199-100X</orcidid></addata></record> |
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| ispartof | Journal of agricultural and food chemistry, 2024-09, Vol.72 (37), p.20273-20285 |
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| subjects | adhesion Agricultural and Environmental Chemistry Bacillus subtilis Bacillus subtilis - genetics Bacillus subtilis - metabolism Bacterial Proteins - chemistry Bacterial Proteins - genetics Bacterial Proteins - metabolism biofilm Biofilms - growth & development biological control biological control agents crown rot DNA DNA-binding domains extracellular matrix food chemistry Fusarium Fusarium - genetics Fusarium - metabolism Fusarium - physiology Gene Expression Regulation, Bacterial mutagenesis mutants operon Plant Diseases - microbiology rhizosphere sporulation transcription factors transcriptomics transposons Triticum - microbiology wheat |
| title | Double-Wing Motif Protein is a Novel Biofilm Regulatory Factor of the Plant Disease Biocontrol Agent, Bacillus subtilis |
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