Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1998 Oct;150(2):687–697. doi: 10.1093/genetics/150.2.687

P-Element insertion at the polyhomeotic gene leads to formation of a novel chimeric protein that negatively regulates yellow gene expression in P-element-induced alleles of Drosophila melanogaster.

T Belenkaya 1, A Soldatov 1, E Nabirochkina 1, I Birjukova 1, S Georgieva 1, P Georgiev 1
PMCID: PMC1460360  PMID: 9755200

Abstract

Polyhomeotic is a member of the Polycomb group (Pc-G) of homeotic repressors. The proteins encoded by the Pc-G genes form repressive complexes on the polycomb group response element sites. The phP1 mutation was induced by insertion of a 1.2-kb P element into the 5' transcribed nontranslated region of the proximal polyhomeotic gene. The phP1 allele confers no mutant phenotype, but represses transcription of P-element-induced alleles at the yellow locus. The phP1 allele encodes a chimeric P-PH protein, consisting of the DNA-binding domain of the P element and the PH protein lacking 12 amino-terminal amino acids. The P-PH, Polycomb (PC), and Posterior sex combs (PSC) proteins were immunohistochemically detected on polytene chromosomes in the regions of P-element insertions.

Full Text

The Full Text of this article is available as a PDF (258.8 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adler P. N., Charlton J., Brunk B. Genetic interactions of the suppressor 2 of zeste region genes. Dev Genet. 1989;10(3):249–260. doi: 10.1002/dvg.1020100314. [DOI] [PubMed] [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  3. Andrews J. D., Gloor G. B. A role for the KP leucine zipper in regulating P element transposition in Drosophila melanogaster. Genetics. 1995 Oct;141(2):587–594. doi: 10.1093/genetics/141.2.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Black D. M., Jackson M. S., Kidwell M. G., Dover G. A. KP elements repress P-induced hybrid dysgenesis in Drosophila melanogaster. EMBO J. 1987 Dec 20;6(13):4125–4135. doi: 10.1002/j.1460-2075.1987.tb02758.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bornemann D., Miller E., Simon J. The Drosophila Polycomb group gene Sex comb on midleg (Scm) encodes a zinc finger protein with similarity to polyhomeotic protein. Development. 1996 May;122(5):1621–1630. doi: 10.1242/dev.122.5.1621. [DOI] [PubMed] [Google Scholar]
  6. Breen T. R., Duncan I. M. Maternal expression of genes that regulate the bithorax complex of Drosophila melanogaster. Dev Biol. 1986 Dec;118(2):442–456. doi: 10.1016/0012-1606(86)90015-1. [DOI] [PubMed] [Google Scholar]
  7. Brunk B. P., Martin E. C., Adler P. N. Molecular genetics of the Posterior sex combs/Suppressor 2 of zeste region of Drosophila: aberrant expression of the Suppressor 2 of zeste gene results in abnormal bristle development. Genetics. 1991 May;128(1):119–132. doi: 10.1093/genetics/128.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chan C. S., Rastelli L., Pirrotta V. A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression. EMBO J. 1994 Jun 1;13(11):2553–2564. doi: 10.1002/j.1460-2075.1994.tb06545.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chiang A., O'Connor M. B., Paro R., Simon J., Bender W. Discrete Polycomb-binding sites in each parasegmental domain of the bithorax complex. Development. 1995 Jun;121(6):1681–1689. doi: 10.1242/dev.121.6.1681. [DOI] [PubMed] [Google Scholar]
  10. DeCamillis M., Cheng N. S., Pierre D., Brock H. W. The polyhomeotic gene of Drosophila encodes a chromatin protein that shares polytene chromosome-binding sites with Polycomb. Genes Dev. 1992 Feb;6(2):223–232. doi: 10.1101/gad.6.2.223. [DOI] [PubMed] [Google Scholar]
  11. Dura J. M., Brock H. W., Santamaria P. Polyhomeotic: a gene of Drosophila melanogaster required for correct expression of segmental identity. Mol Gen Genet. 1985;198(2):213–220. doi: 10.1007/BF00382998. [DOI] [PubMed] [Google Scholar]
  12. Dura J. M., Ingham P. Tissue- and stage-specific control of homeotic and segmentation gene expression in Drosophila embryos by the polyhomeotic gene. Development. 1988 Aug;103(4):733–741. doi: 10.1242/dev.103.4.733. [DOI] [PubMed] [Google Scholar]
  13. Dura J. M., Randsholt N. B., Deatrick J., Erk I., Santamaria P., Freeman J. D., Freeman S. J., Weddell D., Brock H. W. A complex genetic locus, polyhomeotic, is required for segmental specification and epidermal development in D. melanogaster. Cell. 1987 Dec 4;51(5):829–839. doi: 10.1016/0092-8674(87)90106-1. [DOI] [PubMed] [Google Scholar]
  14. Fauvarque M. O., Dura J. M. polyhomeotic regulatory sequences induce developmental regulator-dependent variegation and targeted P-element insertions in Drosophila. Genes Dev. 1993 Aug;7(8):1508–1520. doi: 10.1101/gad.7.8.1508. [DOI] [PubMed] [Google Scholar]
  15. Franke A., DeCamillis M., Zink D., Cheng N., Brock H. W., Paro R. Polycomb and polyhomeotic are constituents of a multimeric protein complex in chromatin of Drosophila melanogaster. EMBO J. 1992 Aug;11(8):2941–2950. doi: 10.1002/j.1460-2075.1992.tb05364.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gaunt S. J., Singh P. B. Homeogene expression patterns and chromosomal imprinting. Trends Genet. 1990 Jul;6(7):208–212. [PubMed] [Google Scholar]
  17. Georgiev P. G., Elagin V. A., Buff E. M., Koliagin N. P. Svoistva supernestabil'nykh mutatsii v lokuse yellow Drosophila melanogaster. Genetika. 1992 Apr;28(4):98–107. [PubMed] [Google Scholar]
  18. Georgiev P., Kozycina M. Interaction between mutations in the suppressor of Hairy wing and modifier of mdg4 genes of Drosophila melanogaster affecting the phenotype of gypsy-induced mutations. Genetics. 1996 Feb;142(2):425–436. doi: 10.1093/genetics/142.2.425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Georgiev P., Tikhomirova T., Yelagin V., Belenkaya T., Gracheva E., Parshikov A., Evgen'ev M. B., Samarina O. P., Corces V. G. Insertions of hybrid P elements in the yellow gene of Drosophila cause a large variety of mutant phenotypes. Genetics. 1997 Jun;146(2):583–594. doi: 10.1093/genetics/146.2.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Geyer P. K., Richardson K. L., Corces V. G., Green M. M. Genetic instability in Drosophila melanogaster: P-element mutagenesis by gene conversion. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6455–6459. doi: 10.1073/pnas.85.17.6455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Geyer P. K., Spana C., Corces V. G. On the molecular mechanism of gypsy-induced mutations at the yellow locus of Drosophila melanogaster. EMBO J. 1986 Oct;5(10):2657–2662. doi: 10.1002/j.1460-2075.1986.tb04548.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hodgson J. W., Cheng N. N., Sinclair D. A., Kyba M., Randsholt N. B., Brock H. W. The polyhomeotic locus of Drosophila melanogaster is transcriptionally and post-transcriptionally regulated during embryogenesis. Mech Dev. 1997 Aug;66(1-2):69–81. doi: 10.1016/s0925-4773(97)00091-9. [DOI] [PubMed] [Google Scholar]
  23. Kassis J. A. Unusual properties of regulatory DNA from the Drosophila engrailed gene: three "pairing-sensitive" sites within a 1.6-kb region. Genetics. 1994 Mar;136(3):1025–1038. doi: 10.1093/genetics/136.3.1025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Locke J., Kotarski M. A., Tartof K. D. Dosage-dependent modifiers of position effect variegation in Drosophila and a mass action model that explains their effect. Genetics. 1988 Sep;120(1):181–198. doi: 10.1093/genetics/120.1.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lonie A., D'Andrea R., Paro R., Saint R. Molecular characterisation of the Polycomblike gene of Drosophila melanogaster, a trans-acting negative regulator of homeotic gene expression. Development. 1994 Sep;120(9):2629–2636. doi: 10.1242/dev.120.9.2629. [DOI] [PubMed] [Google Scholar]
  26. Maes M., Messens E. Phenol as grinding material in RNA preparations. Nucleic Acids Res. 1992 Aug 25;20(16):4374–4374. doi: 10.1093/nar/20.16.4374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Martin E. C., Adler P. N. The Polycomb group gene Posterior Sex Combs encodes a chromosomal protein. Development. 1993 Feb;117(2):641–655. doi: 10.1242/dev.117.2.641. [DOI] [PubMed] [Google Scholar]
  28. Mullis K. B., Faloona F. A. Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 1987;155:335–350. doi: 10.1016/0076-6879(87)55023-6. [DOI] [PubMed] [Google Scholar]
  29. Müller J., Bienz M. Long range repression conferring boundaries of Ultrabithorax expression in the Drosophila embryo. EMBO J. 1991 Nov;10(11):3147–3155. doi: 10.1002/j.1460-2075.1991.tb04876.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nash W. G., Yarkin R. J. Genetic regulation and pattern formation: a study of the yellow locus in Drosophila melanogaster. Genet Res. 1974 Aug;24(1):19–26. doi: 10.1017/s0016672300015044. [DOI] [PubMed] [Google Scholar]
  31. Orlando V., Paro R. Mapping Polycomb-repressed domains in the bithorax complex using in vivo formaldehyde cross-linked chromatin. Cell. 1993 Dec 17;75(6):1187–1198. doi: 10.1016/0092-8674(93)90328-n. [DOI] [PubMed] [Google Scholar]
  32. Parkhurst S. M., Corces V. G. Interactions among the gypsy transposable element and the yellow and the suppressor of hairy-wing loci in Drosophila melanogaster. Mol Cell Biol. 1986 Jan;6(1):47–53. doi: 10.1128/mcb.6.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Paro R., Hogness D. S. The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):263–267. doi: 10.1073/pnas.88.1.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Pirrotta V. PcG complexes and chromatin silencing. Curr Opin Genet Dev. 1997 Apr;7(2):249–258. doi: 10.1016/s0959-437x(97)80135-9. [DOI] [PubMed] [Google Scholar]
  35. Platero J. S., Sharp E. J., Adler P. N., Eissenberg J. C. In vivo assay for protein-protein interactions using Drosophila chromosomes. Chromosoma. 1996 Mar;104(6):393–404. doi: 10.1007/BF00352263. [DOI] [PubMed] [Google Scholar]
  36. Robertson H. M., Preston C. R., Phillis R. W., Johnson-Schlitz D. M., Benz W. K., Engels W. R. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics. 1988 Mar;118(3):461–470. doi: 10.1093/genetics/118.3.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Saiki R. K., Scharf S., Faloona F., Mullis K. B., Horn G. T., Erlich H. A., Arnheim N. Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science. 1985 Dec 20;230(4732):1350–1354. doi: 10.1126/science.2999980. [DOI] [PubMed] [Google Scholar]
  38. Sigrist C. J., Pirrotta V. Chromatin insulator elements block the silencing of a target gene by the Drosophila polycomb response element (PRE) but allow trans interactions between PREs on different chromosomes. Genetics. 1997 Sep;147(1):209–221. doi: 10.1093/genetics/147.1.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Simon J., Chiang A., Bender W., Shimell M. J., O'Connor M. Elements of the Drosophila bithorax complex that mediate repression by Polycomb group products. Dev Biol. 1993 Jul;158(1):131–144. doi: 10.1006/dbio.1993.1174. [DOI] [PubMed] [Google Scholar]
  40. Simon J., Chiang A., Bender W. Ten different Polycomb group genes are required for spatial control of the abdA and AbdB homeotic products. Development. 1992 Feb;114(2):493–505. doi: 10.1242/dev.114.2.493. [DOI] [PubMed] [Google Scholar]
  41. Struhl G. A gene product required for correct initiation of segmental determination in Drosophila. Nature. 1981 Sep 3;293(5827):36–41. doi: 10.1038/293036a0. [DOI] [PubMed] [Google Scholar]
  42. Struhl G., Akam M. Altered distributions of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J. 1985 Dec 1;4(12):3259–3264. doi: 10.1002/j.1460-2075.1985.tb04075.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Strutt H., Cavalli G., Paro R. Co-localization of Polycomb protein and GAGA factor on regulatory elements responsible for the maintenance of homeotic gene expression. EMBO J. 1997 Jun 16;16(12):3621–3632. doi: 10.1093/emboj/16.12.3621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wu C. T., Jones R. S., Lasko P. F., Gelbart W. M. Homeosis and the interaction of zeste and white in Drosophila. Mol Gen Genet. 1989 Sep;218(3):559–564. doi: 10.1007/BF00332424. [DOI] [PubMed] [Google Scholar]
  45. Zink D., Paro R. Drosophila Polycomb-group regulated chromatin inhibits the accessibility of a trans-activator to its target DNA. EMBO J. 1995 Nov 15;14(22):5660–5671. doi: 10.1002/j.1460-2075.1995.tb00253.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES