The post-transcriptional regulator rsmA/csrA activates T3SS by stabilizing the 5' UTR of hrpG, the master regulator of hrp/hrc genes, in Xanthomonas
The RsmA/CsrA family of the post-transcriptional regulators of bacteria is involved in the regulation of many cellular processes, including pathogenesis. In this study, we demonstrated that rsmA not only is required for the full virulence of the phytopathogenic bacterium Xanthomonas citri subsp. cit...
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| description | The RsmA/CsrA family of the post-transcriptional regulators of bacteria is involved in the regulation of many cellular processes, including pathogenesis. In this study, we demonstrated that rsmA not only is required for the full virulence of the phytopathogenic bacterium Xanthomonas citri subsp. citri (XCC) but also contributes to triggering the hypersensitive response (HR) in non-host plants. Deletion of rsmA resulted in significantly reduced virulence in the host plant sweet orange and a delayed and weakened HR in the non-host plant Nicotiana benthamiana. Microarray, quantitative reverse-transcription PCR, western-blotting, and GUS assays indicated that RsmA regulates the expression of the type 3 secretion system (T3SS) at both transcriptional and post-transcriptional levels. The regulation of T3SS by RsmA is a universal phenomenon in T3SS-containing bacteria, but the specific mechanism seems to depend on the interaction between a particular bacterium and its hosts. For Xanthomonads, the mechanism by which RsmA activates T3SS remains unknown. Here, we show that RsmA activates the expression of T3SS-encoding hrp/hrc genes by directly binding to the 5' untranslated region (UTR) of hrpG, the master regulator of the hrp/hrc genes in XCC. RsmA stabilizes hrpG mRNA, leading to increased accumulation of HrpG proteins and subsequently, the activation of hrp/hrc genes. The activation of the hrp/hrc genes by RsmA via HrpG was further supported by the observation that ectopic overexpression of hrpG in an rsmA mutant restored its ability to cause disease in host plants and trigger HR in non-host plants. RsmA also stabilizes the transcripts of another T3SS-associated hrpD operon by directly binding to the 5' UTR region. Taken together, these data revealed that RsmA primarily activates T3SS by acting as a positive regulator of hrpG and that this regulation is critical to the pathogenicity of XCC. |
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In this study, we demonstrated that rsmA not only is required for the full virulence of the phytopathogenic bacterium Xanthomonas citri subsp. citri (XCC) but also contributes to triggering the hypersensitive response (HR) in non-host plants. Deletion of rsmA resulted in significantly reduced virulence in the host plant sweet orange and a delayed and weakened HR in the non-host plant Nicotiana benthamiana. Microarray, quantitative reverse-transcription PCR, western-blotting, and GUS assays indicated that RsmA regulates the expression of the type 3 secretion system (T3SS) at both transcriptional and post-transcriptional levels. The regulation of T3SS by RsmA is a universal phenomenon in T3SS-containing bacteria, but the specific mechanism seems to depend on the interaction between a particular bacterium and its hosts. For Xanthomonads, the mechanism by which RsmA activates T3SS remains unknown. Here, we show that RsmA activates the expression of T3SS-encoding hrp/hrc genes by directly binding to the 5' untranslated region (UTR) of hrpG, the master regulator of the hrp/hrc genes in XCC. RsmA stabilizes hrpG mRNA, leading to increased accumulation of HrpG proteins and subsequently, the activation of hrp/hrc genes. The activation of the hrp/hrc genes by RsmA via HrpG was further supported by the observation that ectopic overexpression of hrpG in an rsmA mutant restored its ability to cause disease in host plants and trigger HR in non-host plants. RsmA also stabilizes the transcripts of another T3SS-associated hrpD operon by directly binding to the 5' UTR region. Taken together, these data revealed that RsmA primarily activates T3SS by acting as a positive regulator of hrpG and that this regulation is critical to the pathogenicity of XCC.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1003945</identifier><identifier>PMID: 24586158</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>5' Untranslated Regions ; Amino Acid Sequence ; Bacteria ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Bacteriology ; Biology ; Blotting, Western ; E coli ; Gene expression ; Gene Expression Regulation, Bacterial - genetics ; Genetic aspects ; Genetic regulation ; Genetic research ; Genetic transcription ; Kinases ; Microbiological research ; Oligonucleotide Array Sequence Analysis ; Pathogenesis ; Plasmids ; Proteins ; Proteobacteria ; Reverse Transcriptase Polymerase Chain Reaction ; Transcription Factors - genetics ; Transcription Factors - metabolism ; Xanthomonas - genetics</subject><ispartof>PLoS pathogens, 2014-02, Vol.10 (2), p.e1003945-e1003945</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Andrade et al 2014 Andrade et al</rights><rights>2014 Andrade et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Andrade MO, Farah CS, Wang N (2014) The Post-transcriptional Regulator rsmA/csrA Activates T3SS by Stabilizing the 5? UTR of hrpG, the Master Regulator of hrp/hrc Genes, in Xanthomonas. PLoS Pathog 10(2): e1003945. doi:10.1371/journal.ppat.1003945</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c633t-4fa1daa9bc0db79860430f2bd4b7818c381c2afb6c5bfdffc0b6209b24ee215a3</citedby><cites>FETCH-LOGICAL-c633t-4fa1daa9bc0db79860430f2bd4b7818c381c2afb6c5bfdffc0b6209b24ee215a3</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/PMC3937308/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3937308/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,2926,23865,27923,27924,53790,53792,79371,79372</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24586158$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Ma, Wenbo</contributor><creatorcontrib>Andrade, Maxuel O</creatorcontrib><creatorcontrib>Farah, Chuck S</creatorcontrib><creatorcontrib>Wang, Nian</creatorcontrib><title>The post-transcriptional regulator rsmA/csrA activates T3SS by stabilizing the 5' UTR of hrpG, the master regulator of hrp/hrc genes, in Xanthomonas</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>The RsmA/CsrA family of the post-transcriptional regulators of bacteria is involved in the regulation of many cellular processes, including pathogenesis. In this study, we demonstrated that rsmA not only is required for the full virulence of the phytopathogenic bacterium Xanthomonas citri subsp. citri (XCC) but also contributes to triggering the hypersensitive response (HR) in non-host plants. Deletion of rsmA resulted in significantly reduced virulence in the host plant sweet orange and a delayed and weakened HR in the non-host plant Nicotiana benthamiana. Microarray, quantitative reverse-transcription PCR, western-blotting, and GUS assays indicated that RsmA regulates the expression of the type 3 secretion system (T3SS) at both transcriptional and post-transcriptional levels. The regulation of T3SS by RsmA is a universal phenomenon in T3SS-containing bacteria, but the specific mechanism seems to depend on the interaction between a particular bacterium and its hosts. For Xanthomonads, the mechanism by which RsmA activates T3SS remains unknown. Here, we show that RsmA activates the expression of T3SS-encoding hrp/hrc genes by directly binding to the 5' untranslated region (UTR) of hrpG, the master regulator of the hrp/hrc genes in XCC. RsmA stabilizes hrpG mRNA, leading to increased accumulation of HrpG proteins and subsequently, the activation of hrp/hrc genes. The activation of the hrp/hrc genes by RsmA via HrpG was further supported by the observation that ectopic overexpression of hrpG in an rsmA mutant restored its ability to cause disease in host plants and trigger HR in non-host plants. RsmA also stabilizes the transcripts of another T3SS-associated hrpD operon by directly binding to the 5' UTR region. Taken together, these data revealed that RsmA primarily activates T3SS by acting as a positive regulator of hrpG and that this regulation is critical to the pathogenicity of XCC.</description><subject>5' Untranslated Regions</subject><subject>Amino Acid Sequence</subject><subject>Bacteria</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacteriology</subject><subject>Biology</subject><subject>Blotting, Western</subject><subject>E coli</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Bacterial - genetics</subject><subject>Genetic aspects</subject><subject>Genetic regulation</subject><subject>Genetic research</subject><subject>Genetic transcription</subject><subject>Kinases</subject><subject>Microbiological research</subject><subject>Oligonucleotide Array Sequence Analysis</subject><subject>Pathogenesis</subject><subject>Plasmids</subject><subject>Proteins</subject><subject>Proteobacteria</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>Xanthomonas - genetics</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVkt2KEzEUgAdR3LX6BqIBL1TYtskkmcncCGXRtbAobLvgXUgyyTRlZjIm6eL6HD6w6c8uLXgjc5Hh5DvfOZycLHuN4AThEk3XbuN70U6GQcQJghBXhD7JzhGleFzikjw9-j_LXoSwhpAgjIrn2VlOKCsQZefZn-VKg8GFOI5e9EF5O0Trkhd43WxaEZ0HPnSzqQp-BoSK9k5EHcASLxZA3oMQhbSt_W37BsSkou_B7fIGOANWfri62MU6EaL2R8L97XTlFWh0r8MFsD34Ifq4cl2qHV5mz4xog351OEfZ7ZfPy8uv4-vvV_PL2fVYFRjHMTEC1UJUUsFalhUrIMHQ5LImsmSIKcyQyoWRhaLS1MYoKIscVjInWueICjzK3u69Q-sCPww0cERhyXBepiKjbL4naifWfPC2E_6eO2H5LuB8w4WPVrWaI0hZjVSpUSWJLpQoKsIYMzVlTGNEk-vTodpGdrpWuk8jb0-kpze9XfHG3XFc4RJDlgQfDgLvfm50iLyzQem2Fb12m13fBBWoLFBC3-3RRqTWbG9cMqotzme4IIwSVG07mvyDSl-tO6tcr41N8ZOEjycJiYn6V2zEJgQ-X9z8B_vtlCV7VnkXgtfmcSoI8u22PzwO3247P2x7SntzPNHHpIf1xn8B6b79AA</recordid><startdate>20140201</startdate><enddate>20140201</enddate><creator>Andrade, Maxuel O</creator><creator>Farah, Chuck S</creator><creator>Wang, Nian</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20140201</creationdate><title>The post-transcriptional regulator rsmA/csrA activates T3SS by stabilizing the 5' UTR of hrpG, the master regulator of hrp/hrc genes, in Xanthomonas</title><author>Andrade, Maxuel O ; Farah, Chuck S ; Wang, Nian</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c633t-4fa1daa9bc0db79860430f2bd4b7818c381c2afb6c5bfdffc0b6209b24ee215a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>5' Untranslated Regions</topic><topic>Amino Acid Sequence</topic><topic>Bacteria</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Bacteriology</topic><topic>Biology</topic><topic>Blotting, Western</topic><topic>E coli</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Bacterial - genetics</topic><topic>Genetic aspects</topic><topic>Genetic regulation</topic><topic>Genetic research</topic><topic>Genetic transcription</topic><topic>Kinases</topic><topic>Microbiological research</topic><topic>Oligonucleotide Array Sequence Analysis</topic><topic>Pathogenesis</topic><topic>Plasmids</topic><topic>Proteins</topic><topic>Proteobacteria</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><topic>Xanthomonas - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Andrade, Maxuel O</creatorcontrib><creatorcontrib>Farah, Chuck S</creatorcontrib><creatorcontrib>Wang, Nian</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Andrade, Maxuel O</au><au>Farah, Chuck S</au><au>Wang, Nian</au><au>Ma, Wenbo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The post-transcriptional regulator rsmA/csrA activates T3SS by stabilizing the 5' UTR of hrpG, the master regulator of hrp/hrc genes, in Xanthomonas</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2014-02-01</date><risdate>2014</risdate><volume>10</volume><issue>2</issue><spage>e1003945</spage><epage>e1003945</epage><pages>e1003945-e1003945</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>The RsmA/CsrA family of the post-transcriptional regulators of bacteria is involved in the regulation of many cellular processes, including pathogenesis. In this study, we demonstrated that rsmA not only is required for the full virulence of the phytopathogenic bacterium Xanthomonas citri subsp. citri (XCC) but also contributes to triggering the hypersensitive response (HR) in non-host plants. Deletion of rsmA resulted in significantly reduced virulence in the host plant sweet orange and a delayed and weakened HR in the non-host plant Nicotiana benthamiana. Microarray, quantitative reverse-transcription PCR, western-blotting, and GUS assays indicated that RsmA regulates the expression of the type 3 secretion system (T3SS) at both transcriptional and post-transcriptional levels. The regulation of T3SS by RsmA is a universal phenomenon in T3SS-containing bacteria, but the specific mechanism seems to depend on the interaction between a particular bacterium and its hosts. For Xanthomonads, the mechanism by which RsmA activates T3SS remains unknown. Here, we show that RsmA activates the expression of T3SS-encoding hrp/hrc genes by directly binding to the 5' untranslated region (UTR) of hrpG, the master regulator of the hrp/hrc genes in XCC. RsmA stabilizes hrpG mRNA, leading to increased accumulation of HrpG proteins and subsequently, the activation of hrp/hrc genes. The activation of the hrp/hrc genes by RsmA via HrpG was further supported by the observation that ectopic overexpression of hrpG in an rsmA mutant restored its ability to cause disease in host plants and trigger HR in non-host plants. RsmA also stabilizes the transcripts of another T3SS-associated hrpD operon by directly binding to the 5' UTR region. Taken together, these data revealed that RsmA primarily activates T3SS by acting as a positive regulator of hrpG and that this regulation is critical to the pathogenicity of XCC.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24586158</pmid><doi>10.1371/journal.ppat.1003945</doi><oa>free_for_read</oa></addata></record> |
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| subjects | 5' Untranslated Regions Amino Acid Sequence Bacteria Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacteriology Biology Blotting, Western E coli Gene expression Gene Expression Regulation, Bacterial - genetics Genetic aspects Genetic regulation Genetic research Genetic transcription Kinases Microbiological research Oligonucleotide Array Sequence Analysis Pathogenesis Plasmids Proteins Proteobacteria Reverse Transcriptase Polymerase Chain Reaction Transcription Factors - genetics Transcription Factors - metabolism Xanthomonas - genetics |
| title | The post-transcriptional regulator rsmA/csrA activates T3SS by stabilizing the 5' UTR of hrpG, the master regulator of hrp/hrc genes, in Xanthomonas |
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