Transvection in the Drosophila Abd-B domain: Extensive upstream sequences are involved in anchoring distant cis-regulatory regions to the promoter

László Sipos, József Mihály, François Karch, Paul Schedl, János Gausz, H. Gyurkovics

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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 front the sequences required for transcription initiation, mediates interactions between the tab 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 tab 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.

Original languageEnglish
Pages (from-to)1031-1050
Number of pages20
JournalGenetics
Volume149
Issue number2
Publication statusPublished - Jun 1998

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Nucleic Acid Regulatory Sequences
Drosophila
Genes
Homeobox Genes
Point Mutation
Diptera
Alleles
Phenotype
Mutation
DNA

ASJC Scopus subject areas

  • Genetics
  • Genetics(clinical)

Cite this

Transvection in the Drosophila Abd-B domain : Extensive upstream sequences are involved in anchoring distant cis-regulatory regions to the promoter. / Sipos, László; Mihály, József; Karch, François; Schedl, Paul; Gausz, János; Gyurkovics, H.

In: Genetics, Vol. 149, No. 2, 06.1998, p. 1031-1050.

Research output: Contribution to journalArticle

Sipos, László ; Mihály, József ; Karch, François ; Schedl, Paul ; Gausz, János ; Gyurkovics, H. / Transvection in the Drosophila Abd-B domain : Extensive upstream sequences are involved in anchoring distant cis-regulatory regions to the promoter. In: Genetics. 1998 ; Vol. 149, No. 2. pp. 1031-1050.
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AU - Gausz, János

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N2 - 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 front the sequences required for transcription initiation, mediates interactions between the tab 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 tab 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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