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Filamentation Regulatory Pathways Control Adhesion-Dependent Surface Responses in Yeast
Signaling pathways can regulate biological responses by the transcriptional regulation of target genes. In yeast, multiple signaling pathways control filamentous growth, a morphogenetic response that occurs in many species including fungal pathogens. Here, we examine the role of signaling pathways t...
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Published in: | Genetics (Austin) 2019-07, Vol.212 (3), p.667-690 |
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description | Signaling pathways can regulate biological responses by the transcriptional regulation of target genes. In yeast, multiple signaling pathways control filamentous growth, a morphogenetic response that occurs in many species including fungal pathogens. Here, we examine the role of signaling pathways that control filamentous growth in regulating adhesion-dependent surface responses, including mat formation and colony patterning. Expression profiling and mutant phenotype analysis showed that the major pathways that regulate filamentous growth [filamentous growth MAPK (fMAPK), RAS, retrograde (RTG), RIM101, RPD3, ELP, SNF1, and PHO85] also regulated mat formation and colony patterning. The chromatin remodeling complex, SAGA, also regulated these responses. We also show that the RAS and RTG pathways coregulated a common set of target genes, and that SAGA regulated target genes known to be controlled by the fMAPK, RAS, and RTG pathways. Analysis of surface growth-specific targets identified genes that respond to low oxygen, high temperature, and desiccation stresses. We also explore the question of why cells make adhesive contacts in colonies. Cell adhesion contacts mediated by the coregulated target and adhesion molecule, Flo11p, deterred entry into colonies by macroscopic predators and impacted colony temperature regulation. The identification of new regulators (
, SAGA), and targets of surface growth in yeast may provide insights into fungal pathogenesis in settings where surface growth and adhesion contributes to virulence. |
doi_str_mv | 10.1534/genetics.119.302004 |
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, SAGA), and targets of surface growth in yeast may provide insights into fungal pathogenesis in settings where surface growth and adhesion contributes to virulence.</description><identifier>ISSN: 1943-2631</identifier><identifier>ISSN: 0016-6731</identifier><identifier>EISSN: 1943-2631</identifier><identifier>DOI: 10.1534/genetics.119.302004</identifier><identifier>PMID: 31053593</identifier><language>eng</language><publisher>United States: Genetics Society of America</publisher><subject>Biofilms ; Cell Adhesion ; Cyclin-Dependent Kinases - genetics ; Cyclin-Dependent Kinases - metabolism ; Gene Expression Regulation, Fungal ; Histone Deacetylases - genetics ; Histone Deacetylases - metabolism ; Hyphae - genetics ; Hyphae - growth & development ; Investigations ; MAP Kinase Signaling System ; Membrane Glycoproteins - genetics ; Membrane Glycoproteins - metabolism ; Protein-Serine-Threonine Kinases - genetics ; Protein-Serine-Threonine Kinases - metabolism ; ras Proteins - genetics ; ras Proteins - metabolism ; Repressor Proteins - genetics ; Repressor Proteins - metabolism ; Saccharomyces cerevisiae - genetics ; Saccharomyces cerevisiae - pathogenicity ; Saccharomyces cerevisiae - physiology ; Saccharomyces cerevisiae Proteins - genetics ; Saccharomyces cerevisiae Proteins - metabolism ; Trans-Activators - genetics ; Trans-Activators - metabolism ; Virulence - genetics</subject><ispartof>Genetics (Austin), 2019-07, Vol.212 (3), p.667-690</ispartof><rights>Copyright © 2019 by the Genetics Society of America.</rights><rights>Copyright © 2019 by the Genetics Society of America 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c405t-f164345b64ea577ba8dab7e3a5996f627babbec474f18a7d3711fc867aba0c653</citedby><cites>FETCH-LOGICAL-c405t-f164345b64ea577ba8dab7e3a5996f627babbec474f18a7d3711fc867aba0c653</cites><orcidid>0000-0003-4371-679X ; 0000-0002-6703-1480 ; 0000-0002-8923-297X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31053593$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chow, Jacky</creatorcontrib><creatorcontrib>Starr, Izzy</creatorcontrib><creatorcontrib>Jamalzadeh, Sheida</creatorcontrib><creatorcontrib>Muniz, Omar</creatorcontrib><creatorcontrib>Kumar, Anuj</creatorcontrib><creatorcontrib>Gokcumen, Omer</creatorcontrib><creatorcontrib>Ferkey, Denise M</creatorcontrib><creatorcontrib>Cullen, Paul J</creatorcontrib><title>Filamentation Regulatory Pathways Control Adhesion-Dependent Surface Responses in Yeast</title><title>Genetics (Austin)</title><addtitle>Genetics</addtitle><description>Signaling pathways can regulate biological responses by the transcriptional regulation of target genes. In yeast, multiple signaling pathways control filamentous growth, a morphogenetic response that occurs in many species including fungal pathogens. Here, we examine the role of signaling pathways that control filamentous growth in regulating adhesion-dependent surface responses, including mat formation and colony patterning. Expression profiling and mutant phenotype analysis showed that the major pathways that regulate filamentous growth [filamentous growth MAPK (fMAPK), RAS, retrograde (RTG), RIM101, RPD3, ELP, SNF1, and PHO85] also regulated mat formation and colony patterning. The chromatin remodeling complex, SAGA, also regulated these responses. We also show that the RAS and RTG pathways coregulated a common set of target genes, and that SAGA regulated target genes known to be controlled by the fMAPK, RAS, and RTG pathways. Analysis of surface growth-specific targets identified genes that respond to low oxygen, high temperature, and desiccation stresses. We also explore the question of why cells make adhesive contacts in colonies. Cell adhesion contacts mediated by the coregulated target and adhesion molecule, Flo11p, deterred entry into colonies by macroscopic predators and impacted colony temperature regulation. The identification of new regulators (
, SAGA), and targets of surface growth in yeast may provide insights into fungal pathogenesis in settings where surface growth and adhesion contributes to virulence.</description><subject>Biofilms</subject><subject>Cell Adhesion</subject><subject>Cyclin-Dependent Kinases - genetics</subject><subject>Cyclin-Dependent Kinases - metabolism</subject><subject>Gene Expression Regulation, Fungal</subject><subject>Histone Deacetylases - genetics</subject><subject>Histone Deacetylases - metabolism</subject><subject>Hyphae - genetics</subject><subject>Hyphae - growth & development</subject><subject>Investigations</subject><subject>MAP Kinase Signaling System</subject><subject>Membrane Glycoproteins - genetics</subject><subject>Membrane Glycoproteins - metabolism</subject><subject>Protein-Serine-Threonine Kinases - genetics</subject><subject>Protein-Serine-Threonine Kinases - metabolism</subject><subject>ras Proteins - genetics</subject><subject>ras Proteins - metabolism</subject><subject>Repressor Proteins - genetics</subject><subject>Repressor Proteins - metabolism</subject><subject>Saccharomyces cerevisiae - genetics</subject><subject>Saccharomyces cerevisiae - pathogenicity</subject><subject>Saccharomyces cerevisiae - physiology</subject><subject>Saccharomyces cerevisiae Proteins - genetics</subject><subject>Saccharomyces cerevisiae Proteins - metabolism</subject><subject>Trans-Activators - genetics</subject><subject>Trans-Activators - metabolism</subject><subject>Virulence - genetics</subject><issn>1943-2631</issn><issn>0016-6731</issn><issn>1943-2631</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNpVkU9LHEEQxRsxuGr8BEKYo5dZu6f_zVwE2UQTEAyaEHJqanpqdifMdq_dPYb99umwruipiqr3XhX8CDlndM4kF5dLdJgGG-eMNXNOK0rFATlmjeBlpTg7fNPPyEmMfyilqpH1EZlxRiWXDT8mv26GEdboEqTBu-IBl9MIyYdt8R3S6i9sY7HwLgU_FtfdCmMWlZ9xg67LnuJxCj1YzLa48S5iLAZX_EaI6SP50MMY8eylnpKfN19-LL6Wd_e33xbXd6UVVKayZ0pwIVslEKTWLdQdtBo5yKZRvarypG3RCi16VoPuuGast7XS0AK1SvJTcrXL3UztGjubvwowmk0Y1hC2xsNg3m_csDJL_2yUYqJudA64eAkI_mnCmMx6iBbHERz6KZqqqpqKcy3rLOU7qQ0-xoD96xlGzX8kZo_EZCRmhyS7Pr398NWzZ8D_AQ7tjLs</recordid><startdate>20190701</startdate><enddate>20190701</enddate><creator>Chow, Jacky</creator><creator>Starr, Izzy</creator><creator>Jamalzadeh, Sheida</creator><creator>Muniz, Omar</creator><creator>Kumar, Anuj</creator><creator>Gokcumen, Omer</creator><creator>Ferkey, Denise M</creator><creator>Cullen, Paul J</creator><general>Genetics Society of America</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>5PM</scope><orcidid>https://orcid.org/0000-0003-4371-679X</orcidid><orcidid>https://orcid.org/0000-0002-6703-1480</orcidid><orcidid>https://orcid.org/0000-0002-8923-297X</orcidid></search><sort><creationdate>20190701</creationdate><title>Filamentation Regulatory Pathways Control Adhesion-Dependent Surface Responses in Yeast</title><author>Chow, Jacky ; Starr, Izzy ; Jamalzadeh, Sheida ; Muniz, Omar ; Kumar, Anuj ; Gokcumen, Omer ; Ferkey, Denise M ; Cullen, Paul J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c405t-f164345b64ea577ba8dab7e3a5996f627babbec474f18a7d3711fc867aba0c653</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Biofilms</topic><topic>Cell Adhesion</topic><topic>Cyclin-Dependent Kinases - genetics</topic><topic>Cyclin-Dependent Kinases - metabolism</topic><topic>Gene Expression Regulation, Fungal</topic><topic>Histone Deacetylases - genetics</topic><topic>Histone Deacetylases - metabolism</topic><topic>Hyphae - genetics</topic><topic>Hyphae - growth & development</topic><topic>Investigations</topic><topic>MAP Kinase Signaling System</topic><topic>Membrane Glycoproteins - genetics</topic><topic>Membrane Glycoproteins - metabolism</topic><topic>Protein-Serine-Threonine Kinases - genetics</topic><topic>Protein-Serine-Threonine Kinases - metabolism</topic><topic>ras Proteins - genetics</topic><topic>ras Proteins - metabolism</topic><topic>Repressor Proteins - genetics</topic><topic>Repressor Proteins - metabolism</topic><topic>Saccharomyces cerevisiae - genetics</topic><topic>Saccharomyces cerevisiae - pathogenicity</topic><topic>Saccharomyces cerevisiae - physiology</topic><topic>Saccharomyces cerevisiae Proteins - genetics</topic><topic>Saccharomyces cerevisiae Proteins - metabolism</topic><topic>Trans-Activators - genetics</topic><topic>Trans-Activators - metabolism</topic><topic>Virulence - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chow, Jacky</creatorcontrib><creatorcontrib>Starr, Izzy</creatorcontrib><creatorcontrib>Jamalzadeh, Sheida</creatorcontrib><creatorcontrib>Muniz, Omar</creatorcontrib><creatorcontrib>Kumar, Anuj</creatorcontrib><creatorcontrib>Gokcumen, Omer</creatorcontrib><creatorcontrib>Ferkey, Denise M</creatorcontrib><creatorcontrib>Cullen, Paul J</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>PubMed Central (Full Participant titles)</collection><jtitle>Genetics (Austin)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chow, Jacky</au><au>Starr, Izzy</au><au>Jamalzadeh, Sheida</au><au>Muniz, Omar</au><au>Kumar, Anuj</au><au>Gokcumen, Omer</au><au>Ferkey, Denise M</au><au>Cullen, Paul J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Filamentation Regulatory Pathways Control Adhesion-Dependent Surface Responses in Yeast</atitle><jtitle>Genetics (Austin)</jtitle><addtitle>Genetics</addtitle><date>2019-07-01</date><risdate>2019</risdate><volume>212</volume><issue>3</issue><spage>667</spage><epage>690</epage><pages>667-690</pages><issn>1943-2631</issn><issn>0016-6731</issn><eissn>1943-2631</eissn><abstract>Signaling pathways can regulate biological responses by the transcriptional regulation of target genes. In yeast, multiple signaling pathways control filamentous growth, a morphogenetic response that occurs in many species including fungal pathogens. Here, we examine the role of signaling pathways that control filamentous growth in regulating adhesion-dependent surface responses, including mat formation and colony patterning. Expression profiling and mutant phenotype analysis showed that the major pathways that regulate filamentous growth [filamentous growth MAPK (fMAPK), RAS, retrograde (RTG), RIM101, RPD3, ELP, SNF1, and PHO85] also regulated mat formation and colony patterning. The chromatin remodeling complex, SAGA, also regulated these responses. We also show that the RAS and RTG pathways coregulated a common set of target genes, and that SAGA regulated target genes known to be controlled by the fMAPK, RAS, and RTG pathways. Analysis of surface growth-specific targets identified genes that respond to low oxygen, high temperature, and desiccation stresses. We also explore the question of why cells make adhesive contacts in colonies. Cell adhesion contacts mediated by the coregulated target and adhesion molecule, Flo11p, deterred entry into colonies by macroscopic predators and impacted colony temperature regulation. The identification of new regulators (
, SAGA), and targets of surface growth in yeast may provide insights into fungal pathogenesis in settings where surface growth and adhesion contributes to virulence.</abstract><cop>United States</cop><pub>Genetics Society of America</pub><pmid>31053593</pmid><doi>10.1534/genetics.119.302004</doi><tpages>24</tpages><orcidid>https://orcid.org/0000-0003-4371-679X</orcidid><orcidid>https://orcid.org/0000-0002-6703-1480</orcidid><orcidid>https://orcid.org/0000-0002-8923-297X</orcidid><oa>free_for_read</oa></addata></record> |
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source | Freely Accessible Science Journals - check A-Z of ejournals; Oxford Journals Online; Alma/SFX Local Collection |
subjects | Biofilms Cell Adhesion Cyclin-Dependent Kinases - genetics Cyclin-Dependent Kinases - metabolism Gene Expression Regulation, Fungal Histone Deacetylases - genetics Histone Deacetylases - metabolism Hyphae - genetics Hyphae - growth & development Investigations MAP Kinase Signaling System Membrane Glycoproteins - genetics Membrane Glycoproteins - metabolism Protein-Serine-Threonine Kinases - genetics Protein-Serine-Threonine Kinases - metabolism ras Proteins - genetics ras Proteins - metabolism Repressor Proteins - genetics Repressor Proteins - metabolism Saccharomyces cerevisiae - genetics Saccharomyces cerevisiae - pathogenicity Saccharomyces cerevisiae - physiology Saccharomyces cerevisiae Proteins - genetics Saccharomyces cerevisiae Proteins - metabolism Trans-Activators - genetics Trans-Activators - metabolism Virulence - genetics |
title | Filamentation Regulatory Pathways Control Adhesion-Dependent Surface Responses in Yeast |
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