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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
Main Authors: Sipos, L, Mihaly, J, Karch, F, Schedl, P, Gausz, J, Gyurkovics, H
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Mihaly, J
Karch, F
Schedl, P
Gausz, J
Gyurkovics, H
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.
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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. 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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. 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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 &amp; 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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.</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>
fulltext fulltext
identifier ISSN: 0016-6731
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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