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Depletion of functional ribosomal RNA operons in Escherichia coli causes increased expression of the remaining intact copies
The synthesis of ribosomal RNA is a complex and highly regulated process. To study this process, we have used deletion‐insertions to disrupt sequentially from one to four of the seven rRNA (rrn) operons on the Escherichia coli genome. Inactivation of four rrn operons caused a 2.3‐fold increase in th...
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Published in: | The EMBO journal 1993-11, Vol.12 (11), p.4305-4315 |
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creator | Condon, C. French, S. Squires, C. Squires, C.L. |
description | The synthesis of ribosomal RNA is a complex and highly regulated process. To study this process, we have used deletion‐insertions to disrupt sequentially from one to four of the seven rRNA (rrn) operons on the Escherichia coli genome. Inactivation of four rrn operons caused a 2.3‐fold increase in the expression of a chloramphenicol acetyl transferase reporter gene fused to the tandem promoters of rrnA and a similar increase in the expression of the trp tRNA gene at the end of rrnC. This reflected enhanced expression of the remaining operons to compensate for having only three intact copies. The elevated expression was caused by an increase in both transcription initiation and RNA polymerase elongation rates specifically on rrn operons and occurred in the absence of changes in the intracellular concentration of ppGpp, suggesting that ppGpp is not involved in the regulation of this phenomenon. We discuss these results in relation to the ribosome feedback inhibition model described by Nomura and coworkers. |
doi_str_mv | 10.1002/j.1460-2075.1993.tb06115.x |
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To study this process, we have used deletion‐insertions to disrupt sequentially from one to four of the seven rRNA (rrn) operons on the Escherichia coli genome. Inactivation of four rrn operons caused a 2.3‐fold increase in the expression of a chloramphenicol acetyl transferase reporter gene fused to the tandem promoters of rrnA and a similar increase in the expression of the trp tRNA gene at the end of rrnC. This reflected enhanced expression of the remaining operons to compensate for having only three intact copies. The elevated expression was caused by an increase in both transcription initiation and RNA polymerase elongation rates specifically on rrn operons and occurred in the absence of changes in the intracellular concentration of ppGpp, suggesting that ppGpp is not involved in the regulation of this phenomenon. 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To study this process, we have used deletion‐insertions to disrupt sequentially from one to four of the seven rRNA (rrn) operons on the Escherichia coli genome. Inactivation of four rrn operons caused a 2.3‐fold increase in the expression of a chloramphenicol acetyl transferase reporter gene fused to the tandem promoters of rrnA and a similar increase in the expression of the trp tRNA gene at the end of rrnC. This reflected enhanced expression of the remaining operons to compensate for having only three intact copies. The elevated expression was caused by an increase in both transcription initiation and RNA polymerase elongation rates specifically on rrn operons and occurred in the absence of changes in the intracellular concentration of ppGpp, suggesting that ppGpp is not involved in the regulation of this phenomenon. We discuss these results in relation to the ribosome feedback inhibition model described by Nomura and coworkers.</description><subject>Bacteriology</subject><subject>Base Sequence</subject><subject>Biological and medical sciences</subject><subject>Cloning, Molecular</subject><subject>DNA, Ribosomal - genetics</subject><subject>DNA, Ribosomal - ultrastructure</subject><subject>DNA-Directed RNA Polymerases - metabolism</subject><subject>Drug Resistance, Microbial - genetics</subject><subject>Escherichia coli</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli - growth & development</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Guanosine Tetraphosphate - metabolism</subject><subject>Metabolism. Enzymes</subject><subject>Microbiology</subject><subject>Models, Genetic</subject><subject>Molecular Sequence Data</subject><subject>Mutagenesis, Insertional</subject><subject>Operon - genetics</subject><subject>RNA, Ribosomal - biosynthesis</subject><subject>Sequence Deletion</subject><subject>Transcription, Genetic</subject><issn>0261-4189</issn><issn>1460-2075</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1993</creationdate><recordtype>article</recordtype><recordid>eNqVkUuLFDEUhYMoYzv6E4Qg4q7KPOopuGjH9sWoILoOSepmOk1VUiZV2gP-eFN20ejSVQ4537n3wkHoCSU5JYQ9P-S0qEjGSF3mtG15PilSUVrmxztoc7buog1hFc0K2rT30YMYD4SQsqnpBbpoGONFQTbo12sYe5isd9gbbGanFy17HKzy0Q9Jffm0xX6E4F3E1uFd1HsIVu-txNr3Fms5R1gsHUBG6DAcxwAxrjOnPeAAg7TOuptETVJPKThaiA_RPSP7CI_W9xJ9e7P7evUuu_789v3V9jrTFSnKrG6ZoabjddEpwlSpdKm6Tpbpo-GcSwXatJw3huoSaNsZ0skkeVOXSrVc8Uv08jR3nNUAnQY3BdmLMdhBhlvhpRX_Os7uxY3_IQrKa1an_LM1H_z3GeIkBhs19L104OcoaNXQgvE2gS9OoA4-xgDmvIMSsVQnDmLpRyz9iKU6sVYnjin8-O8rz9G1q-Q_XX0ZtexNkE7beMZ4XTFeNQnbnrCftofb_zhA7D6--vBH89__H7rL</recordid><startdate>199311</startdate><enddate>199311</enddate><creator>Condon, C.</creator><creator>French, S.</creator><creator>Squires, C.</creator><creator>Squires, C.L.</creator><general>Nature Publishing Group</general><scope>IQODW</scope><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>7QL</scope><scope>7TM</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>5PM</scope></search><sort><creationdate>199311</creationdate><title>Depletion of functional ribosomal RNA operons in Escherichia coli causes increased expression of the remaining intact copies</title><author>Condon, C. ; French, S. ; Squires, C. ; Squires, C.L.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c6045-792f1fd374db02b5bc5bdda53748333abecf9338f1c5e19df0da1c53875bb93b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1993</creationdate><topic>Bacteriology</topic><topic>Base Sequence</topic><topic>Biological and medical sciences</topic><topic>Cloning, Molecular</topic><topic>DNA, Ribosomal - genetics</topic><topic>DNA, Ribosomal - ultrastructure</topic><topic>DNA-Directed RNA Polymerases - metabolism</topic><topic>Drug Resistance, Microbial - genetics</topic><topic>Escherichia coli</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli - growth & development</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Guanosine Tetraphosphate - metabolism</topic><topic>Metabolism. Enzymes</topic><topic>Microbiology</topic><topic>Models, Genetic</topic><topic>Molecular Sequence Data</topic><topic>Mutagenesis, Insertional</topic><topic>Operon - genetics</topic><topic>RNA, Ribosomal - biosynthesis</topic><topic>Sequence Deletion</topic><topic>Transcription, Genetic</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Condon, C.</creatorcontrib><creatorcontrib>French, S.</creatorcontrib><creatorcontrib>Squires, C.</creatorcontrib><creatorcontrib>Squires, C.L.</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The EMBO journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Condon, C.</au><au>French, S.</au><au>Squires, C.</au><au>Squires, C.L.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Depletion of functional ribosomal RNA operons in Escherichia coli causes increased expression of the remaining intact copies</atitle><jtitle>The EMBO journal</jtitle><addtitle>EMBO J</addtitle><date>1993-11</date><risdate>1993</risdate><volume>12</volume><issue>11</issue><spage>4305</spage><epage>4315</epage><pages>4305-4315</pages><issn>0261-4189</issn><eissn>1460-2075</eissn><coden>EMJODG</coden><abstract>The synthesis of ribosomal RNA is a complex and highly regulated process. To study this process, we have used deletion‐insertions to disrupt sequentially from one to four of the seven rRNA (rrn) operons on the Escherichia coli genome. Inactivation of four rrn operons caused a 2.3‐fold increase in the expression of a chloramphenicol acetyl transferase reporter gene fused to the tandem promoters of rrnA and a similar increase in the expression of the trp tRNA gene at the end of rrnC. This reflected enhanced expression of the remaining operons to compensate for having only three intact copies. The elevated expression was caused by an increase in both transcription initiation and RNA polymerase elongation rates specifically on rrn operons and occurred in the absence of changes in the intracellular concentration of ppGpp, suggesting that ppGpp is not involved in the regulation of this phenomenon. 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subjects | Bacteriology Base Sequence Biological and medical sciences Cloning, Molecular DNA, Ribosomal - genetics DNA, Ribosomal - ultrastructure DNA-Directed RNA Polymerases - metabolism Drug Resistance, Microbial - genetics Escherichia coli Escherichia coli - genetics Escherichia coli - growth & development Fundamental and applied biological sciences. Psychology Gene Expression Regulation, Bacterial Guanosine Tetraphosphate - metabolism Metabolism. Enzymes Microbiology Models, Genetic Molecular Sequence Data Mutagenesis, Insertional Operon - genetics RNA, Ribosomal - biosynthesis Sequence Deletion Transcription, Genetic |
title | Depletion of functional ribosomal RNA operons in Escherichia coli causes increased expression of the remaining intact copies |
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