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Transvection in the Drosophila Abd-B domain: extensive upstream sequences are involved in anchoring distant cis-regulatory regions to the promoter
The Abd-B gene, one of the three homeotic genes in the Drosophila bithorax complex (BX-C), is required for the proper identity of the fifth through the eighth abdominal segments (corresponding to parasegments 10-14) of the fruitfly. The morphological difference between these four segments is due to...
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Published in: | Genetics (Austin) 1998-06, Vol.149 (2), p.1031-1050 |
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description | The Abd-B gene, one of the three homeotic genes in the Drosophila bithorax complex (BX-C), is required for the proper identity of the fifth through the eighth abdominal segments (corresponding to parasegments 10-14) of the fruitfly. The morphological difference between these four segments is due to the differential expression of Abd-B, which is achieved by the action of the parasegment-specific cis-regulatory regions infra-abdominal-5 (iab-5), -6, -7 and -8. The dominant gain-of-function mutation Frontabdominal-7 (Fab-7) removes a boundary separating two of these cis-regulatory regions, iab-6 and iab-7. As a consequence of the Fab-7 deletion, the parasegment 12- (PS12-) specific iab-7 is ectopically activated in PS11. This results in the transformation of the sixth abdominal segment (A6) into the seventh (A7) in Fab-7 flies. Here we report that point mutations of the Abd-B gene in trans suppress the Fab-7 phenotype in a pairing-dependent manner and thus represent a type of transvection. We show that the observed suppression is the result of trans-regulation of the defective Abd-B gene by the ectopically activated iab-7. Unlike previously demonstrated cases of trans-regulation in the Abd-B locus, trans-suppression of Fab-7 is sensitive to heterozygosity for chromosomal rearrangements that disturb homologous pairing at the nearby Ubx locus. However, in contrast to Ubx, the transvection we observed in the Abd-B locus is insensitive to the allelic status of zeste. Analysis of different deletion alleles of Abd-B that enhance trans-regulation suggests that an extensive upstream region, different from the sequences required for transcription initiation, mediates interactions between the iab cis-regulatory regions and the proximal Abd-B promoter. Moreover, we find that the amount of DNA deleted in the upstream region is roughly proportional to the strength of trans-interaction, suggesting that this region consists of numerous discrete elements that cooperate in tethering the iab regulatory domains to Abd-B. Possible implications of the tethering complex for the regulation of Abd-B are discussed. In addition, we present evidence that the tenacity of trans-interactions in the Abd-B gene may vary, depending upon the tissue and stage of development. |
doi_str_mv | 10.1093/genetics/149.2.1031 |
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The morphological difference between these four segments is due to the differential expression of Abd-B, which is achieved by the action of the parasegment-specific cis-regulatory regions infra-abdominal-5 (iab-5), -6, -7 and -8. The dominant gain-of-function mutation Frontabdominal-7 (Fab-7) removes a boundary separating two of these cis-regulatory regions, iab-6 and iab-7. As a consequence of the Fab-7 deletion, the parasegment 12- (PS12-) specific iab-7 is ectopically activated in PS11. This results in the transformation of the sixth abdominal segment (A6) into the seventh (A7) in Fab-7 flies. Here we report that point mutations of the Abd-B gene in trans suppress the Fab-7 phenotype in a pairing-dependent manner and thus represent a type of transvection. We show that the observed suppression is the result of trans-regulation of the defective Abd-B gene by the ectopically activated iab-7. Unlike previously demonstrated cases of trans-regulation in the Abd-B locus, trans-suppression of Fab-7 is sensitive to heterozygosity for chromosomal rearrangements that disturb homologous pairing at the nearby Ubx locus. However, in contrast to Ubx, the transvection we observed in the Abd-B locus is insensitive to the allelic status of zeste. Analysis of different deletion alleles of Abd-B that enhance trans-regulation suggests that an extensive upstream region, different from the sequences required for transcription initiation, mediates interactions between the iab cis-regulatory regions and the proximal Abd-B promoter. Moreover, we find that the amount of DNA deleted in the upstream region is roughly proportional to the strength of trans-interaction, suggesting that this region consists of numerous discrete elements that cooperate in tethering the iab regulatory domains to Abd-B. Possible implications of the tethering complex for the regulation of Abd-B are discussed. In addition, we present evidence that the tenacity of trans-interactions in the Abd-B gene may vary, depending upon the tissue and stage of development.</description><identifier>ISSN: 0016-6731</identifier><identifier>ISSN: 1943-2631</identifier><identifier>EISSN: 1943-2631</identifier><identifier>DOI: 10.1093/genetics/149.2.1031</identifier><identifier>PMID: 9611211</identifier><identifier>CODEN: GENTAE</identifier><language>eng</language><publisher>United States: Genetics Soc America</publisher><subject>ABD-B GENE ; ABD-B PROMOTER ; ABDOMEN ; Abdomen - embryology ; Abdomen - innervation ; ALLELES ; ANIMAL CUTICLE ; ANIMAL PROTEINS ; Animals ; Central Nervous System - embryology ; CHEMISTRY ; CHIMIE ; CHROMOSOMAL REARRANGEMENTS ; CUTICULA ANIMAL ; CUTICULE ANIMALE ; DELETIONS ; DNA-Binding Proteins - genetics ; Drosophila - embryology ; Drosophila - genetics ; DROSOPHILA MELANOGASTER ; Drosophila Proteins ; GEN HOMEOTICO ; GENE ; GENE HOMEOTIQUE ; GENES ; Genes, Homeobox ; Genes, Insect ; GENETIC REGULATION ; GENETICA ; GENETICS ; GENETIQUE ; Homeodomain Proteins - genetics ; HOMEOTIC GENES ; IMMUNOHISTOCHEMISTRY ; IMMUNOLOGIE ; IMMUNOLOGY ; INITIATION ; INMUNOLOGIA ; Insects ; INSERTIONAL MUTAGENESIS ; Male ; MUTACION ; MUTATION ; NUCLEOTIDE SEQUENCE ; Phenotype ; Point Mutation ; POINT MUTATIONS ; Promoter Regions, Genetic ; PROTEINAS ; PROTEINE ; PROTEINS ; QUIMICA ; RECOMBINACION ; RECOMBINAISON ; RECOMBINATION ; REGULATORY SEQUENCES ; Regulatory Sequences, Nucleic Acid ; SECUENCIA NUCLEOTIDICA ; Sequence Deletion ; SEQUENCE NUCLEOTIDIQUE ; TRANSCRIPCION ; TRANSCRIPTION ; Translocation, Genetic ; TRANSPOSABLE ELEMENTS</subject><ispartof>Genetics (Austin), 1998-06, Vol.149 (2), p.1031-1050</ispartof><rights>Copyright Genetics Society of America Jun 1998</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c512t-a8c3ce86c372258bcd21cd086617ced50e89173802f514a8c228b2a80b8efa593</citedby><cites>FETCH-LOGICAL-c512t-a8c3ce86c372258bcd21cd086617ced50e89173802f514a8c228b2a80b8efa593</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27923,27924</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/9611211$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sipos, L</creatorcontrib><creatorcontrib>Mihaly, J</creatorcontrib><creatorcontrib>Karch, F</creatorcontrib><creatorcontrib>Schedl, P</creatorcontrib><creatorcontrib>Gausz, J</creatorcontrib><creatorcontrib>Gyurkovics, H</creatorcontrib><title>Transvection in the Drosophila Abd-B domain: extensive upstream sequences are involved in anchoring distant cis-regulatory regions to the promoter</title><title>Genetics (Austin)</title><addtitle>Genetics</addtitle><description>The Abd-B gene, one of the three homeotic genes in the Drosophila bithorax complex (BX-C), is required for the proper identity of the fifth through the eighth abdominal segments (corresponding to parasegments 10-14) of the fruitfly. The morphological difference between these four segments is due to the differential expression of Abd-B, which is achieved by the action of the parasegment-specific cis-regulatory regions infra-abdominal-5 (iab-5), -6, -7 and -8. The dominant gain-of-function mutation Frontabdominal-7 (Fab-7) removes a boundary separating two of these cis-regulatory regions, iab-6 and iab-7. As a consequence of the Fab-7 deletion, the parasegment 12- (PS12-) specific iab-7 is ectopically activated in PS11. This results in the transformation of the sixth abdominal segment (A6) into the seventh (A7) in Fab-7 flies. Here we report that point mutations of the Abd-B gene in trans suppress the Fab-7 phenotype in a pairing-dependent manner and thus represent a type of transvection. We show that the observed suppression is the result of trans-regulation of the defective Abd-B gene by the ectopically activated iab-7. Unlike previously demonstrated cases of trans-regulation in the Abd-B locus, trans-suppression of Fab-7 is sensitive to heterozygosity for chromosomal rearrangements that disturb homologous pairing at the nearby Ubx locus. However, in contrast to Ubx, the transvection we observed in the Abd-B locus is insensitive to the allelic status of zeste. Analysis of different deletion alleles of Abd-B that enhance trans-regulation suggests that an extensive upstream region, different from the sequences required for transcription initiation, mediates interactions between the iab cis-regulatory regions and the proximal Abd-B promoter. Moreover, we find that the amount of DNA deleted in the upstream region is roughly proportional to the strength of trans-interaction, suggesting that this region consists of numerous discrete elements that cooperate in tethering the iab regulatory domains to Abd-B. Possible implications of the tethering complex for the regulation of Abd-B are discussed. In addition, we present evidence that the tenacity of trans-interactions in the Abd-B gene may vary, depending upon the tissue and stage of development.</description><subject>ABD-B GENE</subject><subject>ABD-B PROMOTER</subject><subject>ABDOMEN</subject><subject>Abdomen - embryology</subject><subject>Abdomen - innervation</subject><subject>ALLELES</subject><subject>ANIMAL CUTICLE</subject><subject>ANIMAL PROTEINS</subject><subject>Animals</subject><subject>Central Nervous System - embryology</subject><subject>CHEMISTRY</subject><subject>CHIMIE</subject><subject>CHROMOSOMAL REARRANGEMENTS</subject><subject>CUTICULA ANIMAL</subject><subject>CUTICULE ANIMALE</subject><subject>DELETIONS</subject><subject>DNA-Binding Proteins - genetics</subject><subject>Drosophila - embryology</subject><subject>Drosophila - genetics</subject><subject>DROSOPHILA MELANOGASTER</subject><subject>Drosophila Proteins</subject><subject>GEN HOMEOTICO</subject><subject>GENE</subject><subject>GENE HOMEOTIQUE</subject><subject>GENES</subject><subject>Genes, Homeobox</subject><subject>Genes, Insect</subject><subject>GENETIC REGULATION</subject><subject>GENETICA</subject><subject>GENETICS</subject><subject>GENETIQUE</subject><subject>Homeodomain Proteins - genetics</subject><subject>HOMEOTIC GENES</subject><subject>IMMUNOHISTOCHEMISTRY</subject><subject>IMMUNOLOGIE</subject><subject>IMMUNOLOGY</subject><subject>INITIATION</subject><subject>INMUNOLOGIA</subject><subject>Insects</subject><subject>INSERTIONAL MUTAGENESIS</subject><subject>Male</subject><subject>MUTACION</subject><subject>MUTATION</subject><subject>NUCLEOTIDE SEQUENCE</subject><subject>Phenotype</subject><subject>Point Mutation</subject><subject>POINT MUTATIONS</subject><subject>Promoter Regions, Genetic</subject><subject>PROTEINAS</subject><subject>PROTEINE</subject><subject>PROTEINS</subject><subject>QUIMICA</subject><subject>RECOMBINACION</subject><subject>RECOMBINAISON</subject><subject>RECOMBINATION</subject><subject>REGULATORY SEQUENCES</subject><subject>Regulatory Sequences, Nucleic Acid</subject><subject>SECUENCIA NUCLEOTIDICA</subject><subject>Sequence Deletion</subject><subject>SEQUENCE NUCLEOTIDIQUE</subject><subject>TRANSCRIPCION</subject><subject>TRANSCRIPTION</subject><subject>Translocation, Genetic</subject><subject>TRANSPOSABLE ELEMENTS</subject><issn>0016-6731</issn><issn>1943-2631</issn><issn>1943-2631</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1998</creationdate><recordtype>article</recordtype><recordid>eNptUU1v1DAQjRCoLAu_ACFZHOCU1mMnjsOhUimfUiUOtGfL68wmrhJ7sZ1d-jf4xXjZpQLEySO_N2_ezCuK50BPgbb8rEeHyZp4BlV7yvIfhwfFAtqKl0xweFgsKAVRiobD4-JJjLeUUtHW8qQ4aQUAA1gUP66DdnGLJlnviHUkDUjeBR_9ZrCjJherrnxLOj9p694Q_J7QRbtFMm9iCqgnEvHbjM5gJDpgFtj6cYvdXkk7M_hgXU86G5N2iRgby4D9POrkwx3JZR4aSfK_pm6Cn3zC8LR4tNZjxGfHd1ncfHh_ffmpvPry8fPlxVVpamCp1NJwg1IY3jBWy5XpGJiOSiGgMdjVFGULDZeUrWuoMpsxuWJa0pXEta5bvizOD7qbeTVhZ9CloEe1CXbS4U55bdXfiLOD6v1WQSXo_srL4tVRIPh8hJjUZKPBcdQO_RwViAqA1iITX_5DvPVzcHk5xaACJhq5t8MPJJOvHwOu750AVfu81e-8s4FWMbXPO3e9-HOJ-55jwBl_fcAH2w87G1DFSY9jZoPa7Xb_U1prr3QfbFQ3X6FtG9owyQX_CWyDwxM</recordid><startdate>199806</startdate><enddate>199806</enddate><creator>Sipos, L</creator><creator>Mihaly, J</creator><creator>Karch, F</creator><creator>Schedl, P</creator><creator>Gausz, J</creator><creator>Gyurkovics, H</creator><general>Genetics Soc America</general><general>Genetics Society of America</general><scope>FBQ</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>4T-</scope><scope>4U-</scope><scope>7QP</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>5PM</scope></search><sort><creationdate>199806</creationdate><title>Transvection in the Drosophila Abd-B domain: extensive upstream sequences are involved in anchoring distant cis-regulatory regions to the promoter</title><author>Sipos, L ; Mihaly, J ; Karch, F ; Schedl, P ; Gausz, J ; Gyurkovics, H</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c512t-a8c3ce86c372258bcd21cd086617ced50e89173802f514a8c228b2a80b8efa593</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1998</creationdate><topic>ABD-B GENE</topic><topic>ABD-B PROMOTER</topic><topic>ABDOMEN</topic><topic>Abdomen - embryology</topic><topic>Abdomen - innervation</topic><topic>ALLELES</topic><topic>ANIMAL CUTICLE</topic><topic>ANIMAL PROTEINS</topic><topic>Animals</topic><topic>Central Nervous System - embryology</topic><topic>CHEMISTRY</topic><topic>CHIMIE</topic><topic>CHROMOSOMAL REARRANGEMENTS</topic><topic>CUTICULA ANIMAL</topic><topic>CUTICULE ANIMALE</topic><topic>DELETIONS</topic><topic>DNA-Binding Proteins - genetics</topic><topic>Drosophila - embryology</topic><topic>Drosophila - genetics</topic><topic>DROSOPHILA MELANOGASTER</topic><topic>Drosophila Proteins</topic><topic>GEN HOMEOTICO</topic><topic>GENE</topic><topic>GENE HOMEOTIQUE</topic><topic>GENES</topic><topic>Genes, Homeobox</topic><topic>Genes, Insect</topic><topic>GENETIC REGULATION</topic><topic>GENETICA</topic><topic>GENETICS</topic><topic>GENETIQUE</topic><topic>Homeodomain Proteins - genetics</topic><topic>HOMEOTIC GENES</topic><topic>IMMUNOHISTOCHEMISTRY</topic><topic>IMMUNOLOGIE</topic><topic>IMMUNOLOGY</topic><topic>INITIATION</topic><topic>INMUNOLOGIA</topic><topic>Insects</topic><topic>INSERTIONAL MUTAGENESIS</topic><topic>Male</topic><topic>MUTACION</topic><topic>MUTATION</topic><topic>NUCLEOTIDE SEQUENCE</topic><topic>Phenotype</topic><topic>Point Mutation</topic><topic>POINT MUTATIONS</topic><topic>Promoter Regions, Genetic</topic><topic>PROTEINAS</topic><topic>PROTEINE</topic><topic>PROTEINS</topic><topic>QUIMICA</topic><topic>RECOMBINACION</topic><topic>RECOMBINAISON</topic><topic>RECOMBINATION</topic><topic>REGULATORY SEQUENCES</topic><topic>Regulatory Sequences, Nucleic Acid</topic><topic>SECUENCIA NUCLEOTIDICA</topic><topic>Sequence Deletion</topic><topic>SEQUENCE NUCLEOTIDIQUE</topic><topic>TRANSCRIPCION</topic><topic>TRANSCRIPTION</topic><topic>Translocation, Genetic</topic><topic>TRANSPOSABLE ELEMENTS</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sipos, L</creatorcontrib><creatorcontrib>Mihaly, J</creatorcontrib><creatorcontrib>Karch, F</creatorcontrib><creatorcontrib>Schedl, P</creatorcontrib><creatorcontrib>Gausz, J</creatorcontrib><creatorcontrib>Gyurkovics, H</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</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>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</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>Sipos, L</au><au>Mihaly, J</au><au>Karch, F</au><au>Schedl, P</au><au>Gausz, J</au><au>Gyurkovics, H</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Transvection in the Drosophila Abd-B domain: extensive upstream sequences are involved in anchoring distant cis-regulatory regions to the promoter</atitle><jtitle>Genetics (Austin)</jtitle><addtitle>Genetics</addtitle><date>1998-06</date><risdate>1998</risdate><volume>149</volume><issue>2</issue><spage>1031</spage><epage>1050</epage><pages>1031-1050</pages><issn>0016-6731</issn><issn>1943-2631</issn><eissn>1943-2631</eissn><coden>GENTAE</coden><abstract>The Abd-B gene, one of the three homeotic genes in the Drosophila bithorax complex (BX-C), is required for the proper identity of the fifth through the eighth abdominal segments (corresponding to parasegments 10-14) of the fruitfly. The morphological difference between these four segments is due to the differential expression of Abd-B, which is achieved by the action of the parasegment-specific cis-regulatory regions infra-abdominal-5 (iab-5), -6, -7 and -8. The dominant gain-of-function mutation Frontabdominal-7 (Fab-7) removes a boundary separating two of these cis-regulatory regions, iab-6 and iab-7. As a consequence of the Fab-7 deletion, the parasegment 12- (PS12-) specific iab-7 is ectopically activated in PS11. This results in the transformation of the sixth abdominal segment (A6) into the seventh (A7) in Fab-7 flies. Here we report that point mutations of the Abd-B gene in trans suppress the Fab-7 phenotype in a pairing-dependent manner and thus represent a type of transvection. We show that the observed suppression is the result of trans-regulation of the defective Abd-B gene by the ectopically activated iab-7. Unlike previously demonstrated cases of trans-regulation in the Abd-B locus, trans-suppression of Fab-7 is sensitive to heterozygosity for chromosomal rearrangements that disturb homologous pairing at the nearby Ubx locus. However, in contrast to Ubx, the transvection we observed in the Abd-B locus is insensitive to the allelic status of zeste. Analysis of different deletion alleles of Abd-B that enhance trans-regulation suggests that an extensive upstream region, different from the sequences required for transcription initiation, mediates interactions between the iab cis-regulatory regions and the proximal Abd-B promoter. Moreover, we find that the amount of DNA deleted in the upstream region is roughly proportional to the strength of trans-interaction, suggesting that this region consists of numerous discrete elements that cooperate in tethering the iab regulatory domains to Abd-B. Possible implications of the tethering complex for the regulation of Abd-B are discussed. In addition, we present evidence that the tenacity of trans-interactions in the Abd-B gene may vary, depending upon the tissue and stage of development.</abstract><cop>United States</cop><pub>Genetics Soc America</pub><pmid>9611211</pmid><doi>10.1093/genetics/149.2.1031</doi><tpages>20</tpages><oa>free_for_read</oa></addata></record> |
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ispartof | Genetics (Austin), 1998-06, Vol.149 (2), p.1031-1050 |
issn | 0016-6731 1943-2631 1943-2631 |
language | eng |
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source | Freely Accessible Journals; Oxford Journals Online; Alma/SFX Local Collection |
subjects | ABD-B GENE ABD-B PROMOTER ABDOMEN Abdomen - embryology Abdomen - innervation ALLELES ANIMAL CUTICLE ANIMAL PROTEINS Animals Central Nervous System - embryology CHEMISTRY CHIMIE CHROMOSOMAL REARRANGEMENTS CUTICULA ANIMAL CUTICULE ANIMALE DELETIONS DNA-Binding Proteins - genetics Drosophila - embryology Drosophila - genetics DROSOPHILA MELANOGASTER Drosophila Proteins GEN HOMEOTICO GENE GENE HOMEOTIQUE GENES Genes, Homeobox Genes, Insect GENETIC REGULATION GENETICA GENETICS GENETIQUE Homeodomain Proteins - genetics HOMEOTIC GENES IMMUNOHISTOCHEMISTRY IMMUNOLOGIE IMMUNOLOGY INITIATION INMUNOLOGIA Insects INSERTIONAL MUTAGENESIS Male MUTACION MUTATION NUCLEOTIDE SEQUENCE Phenotype Point Mutation POINT MUTATIONS Promoter Regions, Genetic PROTEINAS PROTEINE PROTEINS QUIMICA RECOMBINACION RECOMBINAISON RECOMBINATION REGULATORY SEQUENCES Regulatory Sequences, Nucleic Acid SECUENCIA NUCLEOTIDICA Sequence Deletion SEQUENCE NUCLEOTIDIQUE TRANSCRIPCION TRANSCRIPTION Translocation, Genetic TRANSPOSABLE ELEMENTS |
title | Transvection in the Drosophila Abd-B domain: extensive upstream sequences are involved in anchoring distant cis-regulatory regions to the promoter |
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