Crossref journal-article
The Company of Biologists
Development (237)
Abstract

Summary Parasegmental (PS)-specific expression of the homeotic genes of the bithorax-complex (BX-C) appears to depend upon the subdivision of the complex into a series of functionally independent cis-regulatory domains. Fab-7 is a regulatory element that lies between iab-6 and iab-7 (the PS11- and PS12-specific cis-regulatory domains, respectively). Deletion of Fab-7 causes ectopic expression of iab- 7 in PS11 (where normally only iab-6 is active). Two models have been proposed to account for the dominant Fab-7 phenotype. The first considers that Fab-7 functions as a boundary element that insulates iab-6 and iab-7. The second model envisages that Fab-7 contains a silencer element that keeps iab-7 repressed in parasegments anterior to PS12. Using a P-element inserted in the middle of the Fab-7 region (the blt transposon), we have generated an extensive collection of new Fab-7 mutations that allow us to subdivide Fab-7 into a boundary element and a Polycomb-respond element (PRE). The boundary lies within 1 kb of DNA on the proximal side of the blt trans- poson (towards iab-6). Deletions removing this element alone cause a complex gain- and loss-of-function phenotype in PS11; in some groups of cells, both iab-6 and iab-7 are active, while in others both iab-6 and iab-7 are inactive. Thus, deletion of the boundary allows activating as well as repressing activities to travel between iab-6 and iab-7. We also provide evidences that the boundary region contains an enhancer blocker element. The Polycomb- response element lies within 0.5 kb of DNA immediately distal to the boundary (towards iab-7). Deletions removing the PRE alone do not typically cause any visible phenotype as homozygotes. Interestingly, weak ectopic activation of iab-7 is observed in hemizygous PRE deletions, suggesting that the mechanisms that keep iab-7 repressed in the absence of this element may depend upon chromosome pairing. These results help to reconcile the previously contradictory models on Fab-7 function and to shed light on how a chromatin domain boundary and a nearby PRE concur in the setting up of the appropriate PS-specific expression of the Abd-B gene of the BX-C.

Bibliography

Mihaly, J., Hogga, I., Gausz, J., Gyurkovics, H., & Karch, F. (1990). In situ dissection of the Fab-7 region of the bithorax complex into a chromatin domain boundary and a Polycomb-response element. Development, 124(9), 1809–1820.

Authors 5
  1. Jozsef Mihaly (first)
  2. Ilham Hogga (additional)
  3. Janos Gausz (additional)
  4. Henrik Gyurkovics (additional)
  5. Frangois Karch (additional)
References 52 Referenced 172
  1. 10.1038/313545a0 / Nature / Segmental distribution of bithorax complex proteins during Drosophila development by Beachy (1985)
  2. 10.1126/science.221.4605.23 / Science / Molecular genetics of the bithorax complex in Drosophila melanogaster by Bender (1983)
  3. 10.1242/dev.111.2.393 / Development / Molecular definition of the morphogenetic and regulatory functions and the cis-regulatory elements of the Drosophila Abd-B homeotic gene by Boulet (1991)
  4. 10.1002/j.1460-2075.1993.tb05785.x / EMBO J. / Silencers in Abdominal-B, a homeotic Drosophila gene by Busturia (1993)
  5. 10.1002/j.1460-2075.1987.tb02619.x / EMBO J. / Double and triple mutant combinations of the bithorax complex of Drosophila by Casanova (1987)
  6. 10.1101/gad.3.9.1424 / Genes Dev. / The molecular genetics of the bithorax complex of Drosophila: characterization of the products of the Abdominal-B domain by Celniker (1989)
  7. 10.1002/j.1460-2075.1990.tb07876.x / EMBO J. / The molecular genetics of the bithorax complex of Drosophila: cis- regulation in the Abdominal-B domain by Celniker (1990)
  8. 10.1002/j.1460-2075.1994.tb06545.x / EMBO J. / A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression by Chan (1994)
  9. 10.1242/dev.121.6.1681 / Development / Discrete Polycomb-binding sites in each parasegmental domain of the bithorax complex by Chiang (1995)
  10. 10.1016/0925-4773(94)90064-7 / Mech. Dev. / Imaginal disc silencers from Ultrabithorax: evidence for Polycomb response elements by Christen (1994)
  11. 10.1016/0092-8674(93)80052-G / Cell / A 5’ element of the chicken beta-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila by Chung (1993)
  12. 10.1146/annurev.ge.21.120187.001441 / Annu. Rev. Genet. / The bithorax complex by Duncan (1987)
  13. 10.1002/j.1460-2075.1993.tb05750.x / EMBO J. / The bluetail transposon: evidence for independent cis-regulatory domains and domain boundaries in the bithorax complex by Galloni (1993)
  14. 10.1093/genetics/139.2.797 / Genetics / Identification of Polycomb and trithorax group responsive elements in the regulatory region of the Drosophila homeotic gene Sex combs reduced by Gindhart (1995)
  15. 10.1002/j.1460-2075.1990.tb07439.x / EMBO J. / A new homeotic mutation in the Drosophila bithorax complex removes a boundary separating two domains of regulation by Gyurkovics (1990)
  16. 10.1101/gad.10.24.3202 / Genes Dev. / Fab-7 functions as a chromatin domain boundary to ensure proper segment specification by the Drosophila bithorax complex by Hagstrom (1996)
  17. 10.1093/genetics/146.4.1365 / Genetics / A Polycomb and GAGA dependent silencer adjoins the Fab-7 boundary in the Drosophila bithorax complex by Hagstrom (1997)
  18. {'key': '2025021402523337600_DEVELOP_124_9_1809C18', 'first-page': '157', 'article-title': 'Targeting a specific deletion, a la Engels, in the Fab-7 boundary ofthe bithorax-complex', 'volume': '76', 'author': 'Hogga', 'year': '1995', 'journal-title': 'Dros. Info. Serv.'} / Dros. Info. Serv. / Targeting a specific deletion, a la Engels, in the Fab-7 boundary ofthe bithorax-complex by Hogga (1995)
  19. 10.1093/genetics/140.2.643 / Genetics / Regulatory regions of the homeotic gene proboscipedia are sensitive to chromosomal pairing by Kapoun (1995)
  20. 10.1016/0092-8674(85)90014-5 / Cell / The abdominal region of the bithorax complex by Karch (1985)
  21. 10.1101/gad.4.9.1573 / Genes Dev. / abdA expression in Drosophila embryos by Karch (1990)
  22. 10.1093/nar/22.15.3138 / Nucleic Acids Res. / Mcp and Fab-7: molecular analysis of putative boundaries of cis- regulatory domains in the bithorax complex of Drosophila melanogaster by Karch (1994)
  23. 10.1093/genetics/136.3.1025 / Genetics / Unusual properties of regulatory DNA from the Drosophila engrailed gene: three ‘pairing-sensitive’ sites within a 1.6-kb region by Kassis (1994)
  24. 10.1016/0092-8674(91)90318-S / Cell / A position-effect assay for boundaries of higher order chromosomal domains by Kellum (1991)
  25. {'key': '2025021402523337600_DEVELOP_124_9_1809C25', 'first-page': '2424', 'article-title': 'A group of scs elements function as domain boundaries in an enhancer- blocking assay', 'volume': '12', 'author': 'Kellum', 'year': '1992', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / A group of scs elements function as domain boundaries in an enhancer- blocking assay by Kellum (1992)
  26. 10.1038/276565a0 / Nature / A gene complex controlling segmentation in Drosophila by Lewis (1978)
  27. {'article-title': 'The genome of Drosophila melanogaster', 'year': '1992', 'author': 'Lindsley', 'key': '2025021402523337600_DEVELOP_124_9_1809C27'} / The genome of Drosophila melanogaster by Lindsley (1992)
  28. 10.1242/dev.110.4.1197 / Development / Expression and regulation of the abd-A gene of Drosophila by Macias (1990)
  29. 10.1093/genetics/138.2.387 / Genetics / Enhancer traps in the Drosophila bithorax complex mark parasegmental domains by McCall (1994)
  30. 10.1002/j.1460-2075.1991.tb04876.x / EMBO J. / Long range repression conferring boundaries of Ultrabithorax expression in the Drosophila embryo by Muller (1991)
  31. 10.1002/j.1460-2075.1992.tb05450.x / EMBO J. / Sharp anterior boundary of homeotic gene expression conferred by the fushi tarazu protein by Muller (1992)
  32. 10.1016/0168-9525(90)90303-N / Trends Genet. / Imprinting a determined state into the chromatin of Drosophila by Paro (1990)
  33. 10.1101/gad.1.9.891 / Genes Dev. / The bithorax complex: control of segmental identity by Peifer (1987)
  34. 10.1002/bies.950160808 / BioEssays / White gene expression, repressive chromatin domains and homeotic gene regulation in Drosophila by Pirrotta (1994)
  35. 10.1002/j.1460-2075.1996.tb00848.x / EMBO J. / Hunchback-independent silencing of late Ubx enhancers by a Polycomb Group Response Element by Poux (1996)
  36. 10.1002/j.1460-2075.1991.tb07662.x / EMBO J. / The bx region enhancer, a distant cis-control element of the Drosophila Ubx gene and its regulation by hunchback and other segmentation genes by Qian (1991)
  37. {'key': '2025021402523337600_DEVELOP_124_9_1809C37', 'article-title': 'Construction and characterization of a TM3 balancer carrying P[(ry+)A2–3] as a stable transposase source', 'volume': '72', 'author': 'Reuter', 'year': '1993', 'journal-title': 'Dros. Info. Serv.'} / Dros. Info. Serv. / Construction and characterization of a TM3 balancer carrying P[(ry+)A2–3] as a stable transposase source by Reuter (1993)
  38. 10.1093/genetics/123.4.815 / Genetics / Modified P elements that mimic the P cytotype in Drosophila melanogaster by Robertson (1989)
  39. 10.1002/j.1460-2075.1993.tb05675.x / EMBO J. / The su(Hw) protein insulates expression of the Drosophila melanogaster white gene from chromosomal position-effects by Roseman (1993)
  40. 10.1038/313108a0 / Nature / Genetic organization of Drosophila bithorax complex by Sanchez-Herrero (1985)
  41. 10.1242/dev.111.2.437 / Development / Control of the expression of the bithorax complex genes abdominal-A and abdominal-B by cis-regulatory regions in Drosophila embryos by Sanchez-Herrero (1991)
  42. 10.1093/genetics/121.3.517 / Genetics / The ash-I, ash-2 and trithorax genes of Drosophila melanogaster are functionally related by Shearn (1989)
  43. 10.1126/science.7909957 / Science / Enhancer point mutation results in a homeotic transformation in Drosophila by Shimell (1994)
  44. 10.1002/j.1460-2075.1990.tb07615.x / EMBO J. / Regulatory elements of the bithorax complex that control expression along the anterior- posterior axis by Simon (1990)
  45. 10.1006/dbio.1993.1174 / Dev. Biol. / Elements of the Drosophila bithorax complex that mediate repression by Polycomb group products by Simon (1993)
  46. 10.1016/0955-0674(95)80093-X / Curr. Opin. Cell Biol. / Locking in stable states of gene expression: transcriptional control during Drosophila development by Simon (1995)
  47. 10.1016/0022-2836(85)90408-5 / J. Mol. Biol. / The 87A7 chromomere. Identification of novel chromatin structures flanking the heat shock locus that may define the boundaries of higher order domains by Udvardy (1985)
  48. 10.1016/0092-8674(84)90202-2 / Cell / Protein products of the bithorax complex in Drosophila by White (1984)
  49. 10.1101/gad.3.12a.1969 / Genes Dev. / The morphogenetic and regulatory functions of the Drosophila Abdominal- B gene are encoded in overlapping RNAs transcribed from separate promoters by Zavortink (1989)
  50. 10.1073/pnas.89.16.7511 / Proc. Natl Acad. Sci. USA / Segmental determination in Drosophila conferred by hunchback (hb), a repressor of the homeotic gene Ultrabithorax (Ubx) by Zhang (1992)
  51. 10.1101/gad.10.24.3195 / Genes Dev. / The Fab-7 element of the bithorax complex attenuates enhancer-promoter interactions in the Drosophila embryo by Zhou (1996)
  52. 10.1002/j.1460-2075.1995.tb00253.x / EMBO J. / Drosophila Polycomb-group regulated chromatin inhibits the accessibility of a trans-activator to its target DNA by Zink (1995)
Dates
Type When
Created 4 years, 4 months ago (April 26, 2021, 12:08 a.m.)
Deposited 6 months, 2 weeks ago (Feb. 13, 2025, 9:52 p.m.)
Indexed 3 weeks, 4 days ago (Aug. 6, 2025, 8:58 a.m.)
Issued 34 years, 9 months ago (Nov. 1, 1990)
Published 34 years, 9 months ago (Nov. 1, 1990)
Published Online 34 years, 9 months ago (Nov. 1, 1990)
Published Print 34 years, 9 months ago (Nov. 1, 1990)
Funders 0

None

@article{Mihaly_1990, title={In situ dissection of the Fab-7 region of the bithorax complex into a chromatin domain boundary and a Polycomb-response element}, volume={124}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.124.9.1809}, DOI={10.1242/dev.124.9.1809}, number={9}, journal={Development}, publisher={The Company of Biologists}, author={Mihaly, Jozsef and Hogga, Ilham and Gausz, Janos and Gyurkovics, Henrik and Karch, Frangois}, year={1990}, month=nov, pages={1809–1820} }