The SWI/SNF chromatin remodeling complex influences transcription by RNA polymerase I in Saccharomyces cerevisiae
SWI/SNF is a chromatin remodeling complex that affects transcription initiation and elongation by RNA polymerase II. Here we report that SWI/SNF also plays a role in transcription by RNA polymerase I (Pol I) in Saccharomyces cerevisiae. Deletion of the genes encoding the Snf6p or Snf5p subunits of S...
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| description | SWI/SNF is a chromatin remodeling complex that affects transcription initiation and elongation by RNA polymerase II. Here we report that SWI/SNF also plays a role in transcription by RNA polymerase I (Pol I) in Saccharomyces cerevisiae. Deletion of the genes encoding the Snf6p or Snf5p subunits of SWI/SNF was lethal in combination with mutations that impair Pol I transcription initiation and elongation. SWI/SNF physically associated with ribosomal DNA (rDNA) within the coding region, with an apparent peak near the 5' end of the gene. In snf6Δ cells there was a ∼2.5-fold reduction in rRNA synthesis rate compared to WT, but there was no change in average polymerase occupancy per gene, the number of rDNA gene repeats, or the percentage of transcriptionally active rDNA genes. However, both ChIP and EM analyses showed a small but reproducible increase in Pol I density in a region near the 5' end of the gene. Based on these data, we conclude that SWI/SNF plays a positive role in Pol I transcription, potentially by modifying chromatin structure in the rDNA repeats. Our findings demonstrate that SWI/SNF influences the most robust transcription machinery in proliferating cells. |
| doi_str_mv | 10.1371/journal.pone.0056793 |
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Here we report that SWI/SNF also plays a role in transcription by RNA polymerase I (Pol I) in Saccharomyces cerevisiae. Deletion of the genes encoding the Snf6p or Snf5p subunits of SWI/SNF was lethal in combination with mutations that impair Pol I transcription initiation and elongation. SWI/SNF physically associated with ribosomal DNA (rDNA) within the coding region, with an apparent peak near the 5' end of the gene. In snf6Δ cells there was a ∼2.5-fold reduction in rRNA synthesis rate compared to WT, but there was no change in average polymerase occupancy per gene, the number of rDNA gene repeats, or the percentage of transcriptionally active rDNA genes. However, both ChIP and EM analyses showed a small but reproducible increase in Pol I density in a region near the 5' end of the gene. Based on these data, we conclude that SWI/SNF plays a positive role in Pol I transcription, potentially by modifying chromatin structure in the rDNA repeats. Our findings demonstrate that SWI/SNF influences the most robust transcription machinery in proliferating cells.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0056793</identifier><identifier>PMID: 23437238</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Biology ; Chromatin ; Chromatin Assembly and Disassembly ; Chromatin remodeling ; Clonal deletion ; Comparative analysis ; Deoxyribonucleic acid ; DNA ; DNA, Ribosomal - metabolism ; DNA-directed RNA polymerase ; Elongation ; Epistasis, Genetic ; Gene Deletion ; Gene Dosage ; Gene Expression Regulation, Fungal ; Genes ; Genetic aspects ; Mutation ; Protein Binding ; Protein Subunits - genetics ; Protein Subunits - metabolism ; Ribonucleic acid ; RNA ; RNA polymerase ; RNA Polymerase I - metabolism ; RNA polymerase II ; RNA, Ribosomal - genetics ; RNA, Ribosomal - metabolism ; rRNA ; Saccharomyces cerevisiae ; Saccharomyces cerevisiae - genetics ; Saccharomyces cerevisiae - metabolism ; Saccharomyces cerevisiae Proteins - genetics ; Saccharomyces cerevisiae Proteins - metabolism ; Transcription (Genetics) ; Transcription elongation ; Transcription initiation ; Transcription, Genetic ; Yeast</subject><ispartof>PloS one, 2013-02, Vol.8 (2), p.e56793</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Zhang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Zhang et al 2013 Zhang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-2b3f017fb20bd21bc964d7c80e26774c994c3a6b6fddb583b3bbeeea3b365eab3</citedby><cites>FETCH-LOGICAL-c692t-2b3f017fb20bd21bc964d7c80e26774c994c3a6b6fddb583b3bbeeea3b365eab3</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/PMC3577654/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3577654/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23437238$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Yinfeng</creatorcontrib><creatorcontrib>Anderson, Susan J</creatorcontrib><creatorcontrib>French, Sarah L</creatorcontrib><creatorcontrib>Sikes, Martha L</creatorcontrib><creatorcontrib>Viktorovskaya, Olga V</creatorcontrib><creatorcontrib>Huband, Jacalyn</creatorcontrib><creatorcontrib>Holcomb, Katherine</creatorcontrib><creatorcontrib>Hartman, 4th, John L</creatorcontrib><creatorcontrib>Beyer, Ann L</creatorcontrib><creatorcontrib>Schneider, David A</creatorcontrib><title>The SWI/SNF chromatin remodeling complex influences transcription by RNA polymerase I in Saccharomyces cerevisiae</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>SWI/SNF is a chromatin remodeling complex that affects transcription initiation and elongation by RNA polymerase II. Here we report that SWI/SNF also plays a role in transcription by RNA polymerase I (Pol I) in Saccharomyces cerevisiae. Deletion of the genes encoding the Snf6p or Snf5p subunits of SWI/SNF was lethal in combination with mutations that impair Pol I transcription initiation and elongation. SWI/SNF physically associated with ribosomal DNA (rDNA) within the coding region, with an apparent peak near the 5' end of the gene. In snf6Δ cells there was a ∼2.5-fold reduction in rRNA synthesis rate compared to WT, but there was no change in average polymerase occupancy per gene, the number of rDNA gene repeats, or the percentage of transcriptionally active rDNA genes. However, both ChIP and EM analyses showed a small but reproducible increase in Pol I density in a region near the 5' end of the gene. Based on these data, we conclude that SWI/SNF plays a positive role in Pol I transcription, potentially by modifying chromatin structure in the rDNA repeats. Our findings demonstrate that SWI/SNF influences the most robust transcription machinery in proliferating cells.</description><subject>Biology</subject><subject>Chromatin</subject><subject>Chromatin Assembly and Disassembly</subject><subject>Chromatin remodeling</subject><subject>Clonal deletion</subject><subject>Comparative analysis</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA, Ribosomal - metabolism</subject><subject>DNA-directed RNA polymerase</subject><subject>Elongation</subject><subject>Epistasis, Genetic</subject><subject>Gene Deletion</subject><subject>Gene Dosage</subject><subject>Gene Expression Regulation, Fungal</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Mutation</subject><subject>Protein Binding</subject><subject>Protein Subunits - genetics</subject><subject>Protein Subunits - metabolism</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA polymerase</subject><subject>RNA Polymerase I - metabolism</subject><subject>RNA polymerase II</subject><subject>RNA, Ribosomal - genetics</subject><subject>RNA, Ribosomal - metabolism</subject><subject>rRNA</subject><subject>Saccharomyces cerevisiae</subject><subject>Saccharomyces cerevisiae - genetics</subject><subject>Saccharomyces cerevisiae - metabolism</subject><subject>Saccharomyces cerevisiae Proteins - genetics</subject><subject>Saccharomyces cerevisiae Proteins - metabolism</subject><subject>Transcription (Genetics)</subject><subject>Transcription elongation</subject><subject>Transcription initiation</subject><subject>Transcription, Genetic</subject><subject>Yeast</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNkl1r2zAYhc3YWLts_2BsgsFgF0llyZbtm0Io6xYoLTTddin08TpWsC1Xskvz76csbolhg-ELCek5Ry_HJ4rex3gR0yw-29rBtaJedLaFBcYpywr6IjqNC0rmjGD68mh_Er3xfhsgmjP2OjohNKEZoflpdH9XAVr_Wp2try-RqpxtRG9a5KCxGmrTbpCyTVfDIzJtWQ_QKvCod6L1ypmuN7ZFcodur5eos_WuASc8oFWA0VooVYlguNtLFDh4MN4IeBu9KkXt4d24zqIfl1_vLr7Pr26-rS6WV3PFCtLPiaQljrNSEiw1iaUqWKIzlWMgLMsSVRSJooJJVmot05xKKiUAiLBhKQhJZ9HHg29XW8_HtDyPKcV5TljIYhatDoS2Yss7ZxrhdtwKw_8cWLfhwvVG1cBFEYYoU50ALRIKpIhzojTDBSRKK733Oh9fG2QDWkEbQqonptOb1lR8Yx84TbOMpUkw-DQaOHs_gO__MfJIbUSYKvwSG8xUY7ziyyTLCU5wQQK1-AsVPg2NUaEvpQnnE8GXiSAwPTz2GzF4z1fr2_9nb35O2c9HbAWi7itv62HfGz8FkwOonPXeQfmcXIz5vu5PafB93flY9yD7cJz6s-ip3_Q3YKr8rA</recordid><startdate>20130220</startdate><enddate>20130220</enddate><creator>Zhang, Yinfeng</creator><creator>Anderson, Susan J</creator><creator>French, Sarah L</creator><creator>Sikes, Martha L</creator><creator>Viktorovskaya, Olga V</creator><creator>Huband, Jacalyn</creator><creator>Holcomb, Katherine</creator><creator>Hartman, 4th, John L</creator><creator>Beyer, Ann L</creator><creator>Schneider, David A</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20130220</creationdate><title>The SWI/SNF chromatin remodeling complex influences transcription by RNA polymerase I in Saccharomyces cerevisiae</title><author>Zhang, Yinfeng ; Anderson, Susan J ; French, Sarah L ; Sikes, Martha L ; Viktorovskaya, Olga V ; Huband, Jacalyn ; Holcomb, Katherine ; Hartman, 4th, John L ; Beyer, Ann L ; Schneider, David A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-2b3f017fb20bd21bc964d7c80e26774c994c3a6b6fddb583b3bbeeea3b365eab3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Biology</topic><topic>Chromatin</topic><topic>Chromatin Assembly and Disassembly</topic><topic>Chromatin remodeling</topic><topic>Clonal deletion</topic><topic>Comparative analysis</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA, Ribosomal - metabolism</topic><topic>DNA-directed RNA polymerase</topic><topic>Elongation</topic><topic>Epistasis, Genetic</topic><topic>Gene Deletion</topic><topic>Gene Dosage</topic><topic>Gene Expression Regulation, Fungal</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Mutation</topic><topic>Protein Binding</topic><topic>Protein Subunits - genetics</topic><topic>Protein Subunits - metabolism</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA polymerase</topic><topic>RNA Polymerase I - metabolism</topic><topic>RNA polymerase II</topic><topic>RNA, Ribosomal - genetics</topic><topic>RNA, Ribosomal - metabolism</topic><topic>rRNA</topic><topic>Saccharomyces cerevisiae</topic><topic>Saccharomyces cerevisiae - genetics</topic><topic>Saccharomyces cerevisiae - metabolism</topic><topic>Saccharomyces cerevisiae Proteins - genetics</topic><topic>Saccharomyces cerevisiae Proteins - metabolism</topic><topic>Transcription (Genetics)</topic><topic>Transcription elongation</topic><topic>Transcription initiation</topic><topic>Transcription, Genetic</topic><topic>Yeast</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Yinfeng</creatorcontrib><creatorcontrib>Anderson, Susan J</creatorcontrib><creatorcontrib>French, Sarah L</creatorcontrib><creatorcontrib>Sikes, Martha L</creatorcontrib><creatorcontrib>Viktorovskaya, Olga V</creatorcontrib><creatorcontrib>Huband, Jacalyn</creatorcontrib><creatorcontrib>Holcomb, Katherine</creatorcontrib><creatorcontrib>Hartman, 4th, John L</creatorcontrib><creatorcontrib>Beyer, Ann L</creatorcontrib><creatorcontrib>Schneider, David A</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: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical 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 Technology 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>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</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>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Here we report that SWI/SNF also plays a role in transcription by RNA polymerase I (Pol I) in Saccharomyces cerevisiae. Deletion of the genes encoding the Snf6p or Snf5p subunits of SWI/SNF was lethal in combination with mutations that impair Pol I transcription initiation and elongation. SWI/SNF physically associated with ribosomal DNA (rDNA) within the coding region, with an apparent peak near the 5' end of the gene. In snf6Δ cells there was a ∼2.5-fold reduction in rRNA synthesis rate compared to WT, but there was no change in average polymerase occupancy per gene, the number of rDNA gene repeats, or the percentage of transcriptionally active rDNA genes. However, both ChIP and EM analyses showed a small but reproducible increase in Pol I density in a region near the 5' end of the gene. Based on these data, we conclude that SWI/SNF plays a positive role in Pol I transcription, potentially by modifying chromatin structure in the rDNA repeats. Our findings demonstrate that SWI/SNF influences the most robust transcription machinery in proliferating cells.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23437238</pmid><doi>10.1371/journal.pone.0056793</doi><tpages>e56793</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Biology Chromatin Chromatin Assembly and Disassembly Chromatin remodeling Clonal deletion Comparative analysis Deoxyribonucleic acid DNA DNA, Ribosomal - metabolism DNA-directed RNA polymerase Elongation Epistasis, Genetic Gene Deletion Gene Dosage Gene Expression Regulation, Fungal Genes Genetic aspects Mutation Protein Binding Protein Subunits - genetics Protein Subunits - metabolism Ribonucleic acid RNA RNA polymerase RNA Polymerase I - metabolism RNA polymerase II RNA, Ribosomal - genetics RNA, Ribosomal - metabolism rRNA Saccharomyces cerevisiae Saccharomyces cerevisiae - genetics Saccharomyces cerevisiae - metabolism Saccharomyces cerevisiae Proteins - genetics Saccharomyces cerevisiae Proteins - metabolism Transcription (Genetics) Transcription elongation Transcription initiation Transcription, Genetic Yeast |
| title | The SWI/SNF chromatin remodeling complex influences transcription by RNA polymerase I in Saccharomyces cerevisiae |
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