Flo11p-Independent Control of "Mat" Formation by Hsp70 Molecular Chaperones and Nucleotide Exchange Factors in Yeast
The yeast Saccharomyces cerevisiae has been used as a model for fungal biofilm formation due to its ability to adhere to plastic surfaces and to form mats on low-density agar petri plates. Mats are complex multicellular structures composed of a network of cables that form a central hub from which em...
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description | The yeast Saccharomyces cerevisiae has been used as a model for fungal biofilm formation due to its ability to adhere to plastic surfaces and to form mats on low-density agar petri plates. Mats are complex multicellular structures composed of a network of cables that form a central hub from which emanate multiple radial spokes. This reproducible and elaborate pattern is indicative of a highly regulated developmental program that depends on specific transcriptional programming, environmental cues, and possibly cell-cell communication systems. While biofilm formation and sliding motility were shown to be strictly dependent on the cell-surface adhesin Flo11p, little is known about the cellular machinery that controls mat formation. Here we show that Hsp70 molecular chaperones play key roles in this process with the assistance of the nucleotide exchange factors Fes1p and Sse1p and the Hsp40 family member Ydj1p. The disruption of these cofactors completely abolished mat formation. Furthermore, complex interactions among SSA genes were observed: mat formation depended mostly on SSA1 while minor defects were observed upon loss of SSA2; additional mutations in SSA3 or SSA4 further enhanced these phenotypes. Importantly, these mutations did not compromise invasive growth or Flo11p expression, suggesting that Flo11p-independent pathways are necessary to form mats. |
doi_str_mv | 10.1534/genetics.107.081141 |
format | Article |
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Mats are complex multicellular structures composed of a network of cables that form a central hub from which emanate multiple radial spokes. This reproducible and elaborate pattern is indicative of a highly regulated developmental program that depends on specific transcriptional programming, environmental cues, and possibly cell-cell communication systems. While biofilm formation and sliding motility were shown to be strictly dependent on the cell-surface adhesin Flo11p, little is known about the cellular machinery that controls mat formation. Here we show that Hsp70 molecular chaperones play key roles in this process with the assistance of the nucleotide exchange factors Fes1p and Sse1p and the Hsp40 family member Ydj1p. The disruption of these cofactors completely abolished mat formation. Furthermore, complex interactions among SSA genes were observed: mat formation depended mostly on SSA1 while minor defects were observed upon loss of SSA2; additional mutations in SSA3 or SSA4 further enhanced these phenotypes. Importantly, these mutations did not compromise invasive growth or Flo11p expression, suggesting that Flo11p-independent pathways are necessary to form mats.</description><identifier>ISSN: 0016-6731</identifier><identifier>ISSN: 1943-2631</identifier><identifier>EISSN: 1943-2631</identifier><identifier>DOI: 10.1534/genetics.107.081141</identifier><identifier>PMID: 17947402</identifier><identifier>CODEN: GENTAE</identifier><language>eng</language><publisher>United States: Genetics Soc America</publisher><subject>Bacterial Adhesion ; Biochemistry, Molecular Biology ; Biofilms ; Biofilms - growth & development ; Cells ; Genes, Fungal ; HSP110 Heat-Shock Proteins ; HSP110 Heat-Shock Proteins - genetics ; HSP110 Heat-Shock Proteins - physiology ; HSP40 Heat-Shock Proteins ; HSP40 Heat-Shock Proteins - genetics ; HSP40 Heat-Shock Proteins - physiology ; HSP70 Heat-Shock Proteins ; HSP70 Heat-Shock Proteins - genetics ; HSP70 Heat-Shock Proteins - physiology ; Intracellular Signaling Peptides and Proteins ; Intracellular Signaling Peptides and Proteins - genetics ; Intracellular Signaling Peptides and Proteins - physiology ; Investigations ; Kinases ; Life Sciences ; Membrane Glycoproteins ; Membrane Proteins ; Membrane Proteins - genetics ; Membrane Proteins - physiology ; Models, Biological ; Molecular biology ; Mutation ; Quality control ; Saccharomyces cerevisiae ; Saccharomyces cerevisiae - genetics ; Saccharomyces cerevisiae - physiology ; Saccharomyces cerevisiae Proteins ; Saccharomyces cerevisiae Proteins - genetics ; Saccharomyces cerevisiae Proteins - physiology ; Signal transduction</subject><ispartof>Genetics (Austin), 2007-11, Vol.177 (3), p.1679-1689</ispartof><rights>Copyright Genetics Society of America Nov 2007</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>Copyright © 2007 by the Genetics Society of America</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c496t-4f55ac10c448dbad4f71adff47c276ec0e2edcd2627ed2aa8cdfa325a31e70d33</citedby><cites>FETCH-LOGICAL-c496t-4f55ac10c448dbad4f71adff47c276ec0e2edcd2627ed2aa8cdfa325a31e70d33</cites><orcidid>0000-0001-7440-6394</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/17947402$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-00315527$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Martineau, Celine N</creatorcontrib><creatorcontrib>Beckerich, Jean-Marie</creatorcontrib><creatorcontrib>Kabani, Mehdi</creatorcontrib><title>Flo11p-Independent Control of "Mat" Formation by Hsp70 Molecular Chaperones and Nucleotide Exchange Factors in Yeast</title><title>Genetics (Austin)</title><addtitle>Genetics</addtitle><description>The yeast Saccharomyces cerevisiae has been used as a model for fungal biofilm formation due to its ability to adhere to plastic surfaces and to form mats on low-density agar petri plates. Mats are complex multicellular structures composed of a network of cables that form a central hub from which emanate multiple radial spokes. This reproducible and elaborate pattern is indicative of a highly regulated developmental program that depends on specific transcriptional programming, environmental cues, and possibly cell-cell communication systems. While biofilm formation and sliding motility were shown to be strictly dependent on the cell-surface adhesin Flo11p, little is known about the cellular machinery that controls mat formation. Here we show that Hsp70 molecular chaperones play key roles in this process with the assistance of the nucleotide exchange factors Fes1p and Sse1p and the Hsp40 family member Ydj1p. The disruption of these cofactors completely abolished mat formation. Furthermore, complex interactions among SSA genes were observed: mat formation depended mostly on SSA1 while minor defects were observed upon loss of SSA2; additional mutations in SSA3 or SSA4 further enhanced these phenotypes. Importantly, these mutations did not compromise invasive growth or Flo11p expression, suggesting that Flo11p-independent pathways are necessary to form mats.</description><subject>Bacterial Adhesion</subject><subject>Biochemistry, Molecular Biology</subject><subject>Biofilms</subject><subject>Biofilms - growth & development</subject><subject>Cells</subject><subject>Genes, Fungal</subject><subject>HSP110 Heat-Shock Proteins</subject><subject>HSP110 Heat-Shock Proteins - genetics</subject><subject>HSP110 Heat-Shock Proteins - physiology</subject><subject>HSP40 Heat-Shock Proteins</subject><subject>HSP40 Heat-Shock Proteins - genetics</subject><subject>HSP40 Heat-Shock Proteins - physiology</subject><subject>HSP70 Heat-Shock Proteins</subject><subject>HSP70 Heat-Shock Proteins - genetics</subject><subject>HSP70 Heat-Shock Proteins - physiology</subject><subject>Intracellular Signaling Peptides and Proteins</subject><subject>Intracellular Signaling Peptides and Proteins - genetics</subject><subject>Intracellular Signaling Peptides and Proteins - physiology</subject><subject>Investigations</subject><subject>Kinases</subject><subject>Life Sciences</subject><subject>Membrane Glycoproteins</subject><subject>Membrane Proteins</subject><subject>Membrane Proteins - genetics</subject><subject>Membrane Proteins - physiology</subject><subject>Models, Biological</subject><subject>Molecular biology</subject><subject>Mutation</subject><subject>Quality control</subject><subject>Saccharomyces cerevisiae</subject><subject>Saccharomyces cerevisiae - genetics</subject><subject>Saccharomyces cerevisiae - physiology</subject><subject>Saccharomyces cerevisiae Proteins</subject><subject>Saccharomyces cerevisiae Proteins - genetics</subject><subject>Saccharomyces cerevisiae Proteins - physiology</subject><subject>Signal transduction</subject><issn>0016-6731</issn><issn>1943-2631</issn><issn>1943-2631</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2007</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>BENPR</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNpdkV-PEyEUxSdG49bVT2BiSB80PkzlAgOdF5NNs7WbdPVFH3wiFJh2NhRGYLbut5em9d--QHL5nXtyOFX1GvAMGso-bK23uddpBljM8ByAwZNqAi2jNeEUnlYTjIHXXFC4qF6kdIcx5m0zf15dgGiZYJhMqrx0AWCob7yxgy2Hz2gRfI7BodCh6a3KU7QMca9yHzzaPKBVGgRGt8FZPToV0WKnBhuDtwkpb9DnUTsbcm8suv6pd8pvLVoqnUNMqPfou1Upv6yedcol--p8X1bfltdfF6t6_eXTzeJqXWvW8lyzrmmUBqwZm5uNMqwToEzXMaGJ4FZjS6zRhnAirCFKzbXpFCWNomAFNpReVh9Pe4dxsy9oCReVk0Ps9yo-yKB6-f-L73dyG-4lASZazsuC96cFu0ey1dVaHmcYU2gaIu6hsG_PZjH8GG3Kct8nbZ1T3oYxST5vWAkiCjh9BN6FMfryEUdfoIKSI0RPkI4hpWi7P_aA5bF--bv-MhDyVH9Rvfk38F_Nue8CvDsH6re7Qx-tTHvlXMFBHg4HEEJSCVy09Bf5sbwP</recordid><startdate>20071101</startdate><enddate>20071101</enddate><creator>Martineau, Celine N</creator><creator>Beckerich, Jean-Marie</creator><creator>Kabani, Mehdi</creator><general>Genetics Soc America</general><general>Genetics Society of America</general><general>Oxford University Press</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>3V.</scope><scope>4T-</scope><scope>4U-</scope><scope>7QP</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K9-</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0R</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7440-6394</orcidid></search><sort><creationdate>20071101</creationdate><title>Flo11p-Independent Control of "Mat" Formation by Hsp70 Molecular Chaperones and Nucleotide Exchange Factors in Yeast</title><author>Martineau, Celine N ; Beckerich, Jean-Marie ; Kabani, Mehdi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c496t-4f55ac10c448dbad4f71adff47c276ec0e2edcd2627ed2aa8cdfa325a31e70d33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2007</creationdate><topic>Bacterial Adhesion</topic><topic>Biochemistry, Molecular Biology</topic><topic>Biofilms</topic><topic>Biofilms - growth & development</topic><topic>Cells</topic><topic>Genes, Fungal</topic><topic>HSP110 Heat-Shock Proteins</topic><topic>HSP110 Heat-Shock Proteins - genetics</topic><topic>HSP110 Heat-Shock Proteins - physiology</topic><topic>HSP40 Heat-Shock Proteins</topic><topic>HSP40 Heat-Shock Proteins - genetics</topic><topic>HSP40 Heat-Shock Proteins - physiology</topic><topic>HSP70 Heat-Shock Proteins</topic><topic>HSP70 Heat-Shock Proteins - genetics</topic><topic>HSP70 Heat-Shock Proteins - physiology</topic><topic>Intracellular Signaling Peptides and Proteins</topic><topic>Intracellular Signaling Peptides and Proteins - genetics</topic><topic>Intracellular Signaling Peptides and Proteins - physiology</topic><topic>Investigations</topic><topic>Kinases</topic><topic>Life Sciences</topic><topic>Membrane Glycoproteins</topic><topic>Membrane Proteins</topic><topic>Membrane Proteins - genetics</topic><topic>Membrane Proteins - physiology</topic><topic>Models, Biological</topic><topic>Molecular biology</topic><topic>Mutation</topic><topic>Quality control</topic><topic>Saccharomyces cerevisiae</topic><topic>Saccharomyces cerevisiae - genetics</topic><topic>Saccharomyces cerevisiae - physiology</topic><topic>Saccharomyces cerevisiae Proteins</topic><topic>Saccharomyces cerevisiae Proteins - genetics</topic><topic>Saccharomyces cerevisiae Proteins - physiology</topic><topic>Signal transduction</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Martineau, Celine N</creatorcontrib><creatorcontrib>Beckerich, Jean-Marie</creatorcontrib><creatorcontrib>Kabani, Mehdi</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Docstoc</collection><collection>University Readers</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>SciTech Premium Collection</collection><collection>Consumer Health Database (Alumni Edition)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Consumer Health Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Research Library</collection><collection>Science Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Research Library (Corporate)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</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>Martineau, Celine N</au><au>Beckerich, Jean-Marie</au><au>Kabani, Mehdi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Flo11p-Independent Control of "Mat" Formation by Hsp70 Molecular Chaperones and Nucleotide Exchange Factors in Yeast</atitle><jtitle>Genetics (Austin)</jtitle><addtitle>Genetics</addtitle><date>2007-11-01</date><risdate>2007</risdate><volume>177</volume><issue>3</issue><spage>1679</spage><epage>1689</epage><pages>1679-1689</pages><issn>0016-6731</issn><issn>1943-2631</issn><eissn>1943-2631</eissn><coden>GENTAE</coden><abstract>The yeast Saccharomyces cerevisiae has been used as a model for fungal biofilm formation due to its ability to adhere to plastic surfaces and to form mats on low-density agar petri plates. Mats are complex multicellular structures composed of a network of cables that form a central hub from which emanate multiple radial spokes. This reproducible and elaborate pattern is indicative of a highly regulated developmental program that depends on specific transcriptional programming, environmental cues, and possibly cell-cell communication systems. While biofilm formation and sliding motility were shown to be strictly dependent on the cell-surface adhesin Flo11p, little is known about the cellular machinery that controls mat formation. Here we show that Hsp70 molecular chaperones play key roles in this process with the assistance of the nucleotide exchange factors Fes1p and Sse1p and the Hsp40 family member Ydj1p. The disruption of these cofactors completely abolished mat formation. Furthermore, complex interactions among SSA genes were observed: mat formation depended mostly on SSA1 while minor defects were observed upon loss of SSA2; additional mutations in SSA3 or SSA4 further enhanced these phenotypes. Importantly, these mutations did not compromise invasive growth or Flo11p expression, suggesting that Flo11p-independent pathways are necessary to form mats.</abstract><cop>United States</cop><pub>Genetics Soc America</pub><pmid>17947402</pmid><doi>10.1534/genetics.107.081141</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0001-7440-6394</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Bacterial Adhesion Biochemistry, Molecular Biology Biofilms Biofilms - growth & development Cells Genes, Fungal HSP110 Heat-Shock Proteins HSP110 Heat-Shock Proteins - genetics HSP110 Heat-Shock Proteins - physiology HSP40 Heat-Shock Proteins HSP40 Heat-Shock Proteins - genetics HSP40 Heat-Shock Proteins - physiology HSP70 Heat-Shock Proteins HSP70 Heat-Shock Proteins - genetics HSP70 Heat-Shock Proteins - physiology Intracellular Signaling Peptides and Proteins Intracellular Signaling Peptides and Proteins - genetics Intracellular Signaling Peptides and Proteins - physiology Investigations Kinases Life Sciences Membrane Glycoproteins Membrane Proteins Membrane Proteins - genetics Membrane Proteins - physiology Models, Biological Molecular biology Mutation Quality control Saccharomyces cerevisiae Saccharomyces cerevisiae - genetics Saccharomyces cerevisiae - physiology Saccharomyces cerevisiae Proteins Saccharomyces cerevisiae Proteins - genetics Saccharomyces cerevisiae Proteins - physiology Signal transduction |
title | Flo11p-Independent Control of "Mat" Formation by Hsp70 Molecular Chaperones and Nucleotide Exchange Factors in Yeast |
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