Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1994 Apr;136(4):1341–1353. doi: 10.1093/genetics/136.4.1341

A Role of Polycomb Group Genes in the Regulation of Gap Gene Expression in Drosophila

F Pelegri 1, R Lehmann 1
PMCID: PMC1205915  PMID: 8013911

Abstract

Anteroposterior polarity of the Drosophila embryo is initiated by the localized activities of the maternal genes, bicoid and nanos, which establish a gradient of the hunchback (hb) morphogen. nanos determines the distribution of the maternal Hb protein by regulating its translation. To identify further components of this pathway we isolated suppressors of nanos. In the absence of nanos high levels of Hb protein repress the abdomen-specific genes knirps and giant. In suppressor-of-nanos mutants, knirps and giant are expressed in spite of high Hb levels. The suppressors are alleles of Enhancer of zeste (E(z)) a member of the Polycomb group (Pc-G) of genes. We show that E(z), and likely other Pc-G genes, are required for maintaining the expression domains of knirps and giant initiated by the maternal Hb protein gradient. We have identified a small region of the knirps promoter that mediates the regulation by E(z) and hb. Because Pc-G genes are thought to control gene expression by regulating chromatin, we propose that imprinting at the chromatin level underlies the determination of anteroposterior polarity in the early embryo.

Full Text

The Full Text of this article is available as a PDF (8.1 MB).

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. Barker D. D., Wang C., Moore J., Dickinson L. K., Lehmann R. Pumilio is essential for function but not for distribution of the Drosophila abdominal determinant Nanos. Genes Dev. 1992 Dec;6(12A):2312–2326. doi: 10.1101/gad.6.12a.2312. [DOI] [PubMed] [Google Scholar]
  3. Berleth T., Burri M., Thoma G., Bopp D., Richstein S., Frigerio G., Noll M., Nüsslein-Volhard C. The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. EMBO J. 1988 Jun;7(6):1749–1756. doi: 10.1002/j.1460-2075.1988.tb03004.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. Capovilla M., Eldon E. D., Pirrotta V. The giant gene of Drosophila encodes a b-ZIP DNA-binding protein that regulates the expression of other segmentation gap genes. Development. 1992 Jan;114(1):99–112. doi: 10.1242/dev.114.1.99. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Donoghue M. J., Patton B. L., Sanes J. R., Merlie J. P. An axial gradient of transgene methylation in murine skeletal muscle: genomic imprint of rostrocaudal position. Development. 1992 Dec;116(4):1101–1112. doi: 10.1242/dev.116.4.1101. [DOI] [PubMed] [Google Scholar]
  9. Doyle H. J., Bishop J. M. Torso, a receptor tyrosine kinase required for embryonic pattern formation, shares substrates with the sevenless and EGF-R pathways in Drosophila. Genes Dev. 1993 Apr;7(4):633–646. doi: 10.1101/gad.7.4.633. [DOI] [PubMed] [Google Scholar]
  10. Doyle H. J., Kraut R., Levine M. Spatial regulation of zerknüllt: a dorsal-ventral patterning gene in Drosophila. Genes Dev. 1989 Oct;3(10):1518–1533. doi: 10.1101/gad.3.10.1518. [DOI] [PubMed] [Google Scholar]
  11. Driever W., Nüsslein-Volhard C. The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo. Nature. 1989 Jan 12;337(6203):138–143. doi: 10.1038/337138a0. [DOI] [PubMed] [Google Scholar]
  12. Driever W., Thoma G., Nüsslein-Volhard C. Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen. Nature. 1989 Aug 3;340(6232):363–367. doi: 10.1038/340363a0. [DOI] [PubMed] [Google Scholar]
  13. Driever W., Thoma G., Nüsslein-Volhard C. Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen. Nature. 1989 Aug 3;340(6232):363–367. doi: 10.1038/340363a0. [DOI] [PubMed] [Google Scholar]
  14. Duncan I. M. Polycomblike: a gene that appears to be required for the normal expression of the bithorax and antennapedia gene complexes of Drosophila melanogaster. Genetics. 1982 Sep;102(1):49–70. doi: 10.1093/genetics/102.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Eldon E. D., Pirrotta V. Interactions of the Drosophila gap gene giant with maternal and zygotic pattern-forming genes. Development. 1991 Feb;111(2):367–378. doi: 10.1242/dev.111.2.367. [DOI] [PubMed] [Google Scholar]
  18. Foe V. E., Alberts B. M. Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci. 1983 May;61:31–70. doi: 10.1242/jcs.61.1.31. [DOI] [PubMed] [Google Scholar]
  19. Fuller M. T., Regan C. L., Green L. L., Robertson B., Deuring R., Hays T. S. Interacting genes identify interacting proteins involved in microtubule function in Drosophila. Cell Motil Cytoskeleton. 1989;14(1):128–135. doi: 10.1002/cm.970140122. [DOI] [PubMed] [Google Scholar]
  20. Gavis E. R., Lehmann R. Localization of nanos RNA controls embryonic polarity. Cell. 1992 Oct 16;71(2):301–313. doi: 10.1016/0092-8674(92)90358-j. [DOI] [PubMed] [Google Scholar]
  21. Glicksman M. A., Brower D. L. Persistent ectopic expression of Drosophila homeotic genes resulting from maternal deficiency of the extra sex combs gene product. Dev Biol. 1990 Dec;142(2):422–431. doi: 10.1016/0012-1606(90)90364-o. [DOI] [PubMed] [Google Scholar]
  22. Haynie J. L. The maternal and zygotic roles of the gene Polycomb in embryonic determination in Drosophila melanogaster. Dev Biol. 1983 Dec;100(2):399–411. doi: 10.1016/0012-1606(83)90234-8. [DOI] [PubMed] [Google Scholar]
  23. Hülskamp M., Pfeifle C., Tautz D. A morphogenetic gradient of hunchback protein organizes the expression of the gap genes Krüppel and knirps in the early Drosophila embryo. Nature. 1990 Aug 9;346(6284):577–580. doi: 10.1038/346577a0. [DOI] [PubMed] [Google Scholar]
  24. Hülskamp M., Tautz D. Gap genes and gradients--the logic behind the gaps. Bioessays. 1991 Jun;13(6):261–268. doi: 10.1002/bies.950130602. [DOI] [PubMed] [Google Scholar]
  25. Ingham P. W. A gene that regulates the bithorax complex differentially in larval and adult cells of Drosophila. Cell. 1984 Jul;37(3):815–823. doi: 10.1016/0092-8674(84)90416-1. [DOI] [PubMed] [Google Scholar]
  26. Irish V. F., Martinez-Arias A., Akam M. Spatial regulation of the Antennapedia and Ultrabithorax homeotic genes during Drosophila early development. EMBO J. 1989 May;8(5):1527–1537. doi: 10.1002/j.1460-2075.1989.tb03537.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Irish V., Lehmann R., Akam M. The Drosophila posterior-group gene nanos functions by repressing hunchback activity. Nature. 1989 Apr 20;338(6217):646–648. doi: 10.1038/338646a0. [DOI] [PubMed] [Google Scholar]
  28. Jones R. S., Gelbart W. M. The Drosophila Polycomb-group gene Enhancer of zeste contains a region with sequence similarity to trithorax. Mol Cell Biol. 1993 Oct;13(10):6357–6366. doi: 10.1128/mcb.13.10.6357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kennison J. A., Russell M. A. Dosage-Dependent Modifiers of Homoeotic Mutations in Drosophila melanogaster. Genetics. 1987 May;116(1):75–86. doi: 10.1093/genetics/116.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kennison J. A., Tamkun J. W. Dosage-dependent modifiers of polycomb and antennapedia mutations in Drosophila. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8136–8140. doi: 10.1073/pnas.85.21.8136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kennison J. A., Tamkun J. W. Trans-regulation of homeotic genes in Drosophila. New Biol. 1992 Feb;4(2):91–96. [PubMed] [Google Scholar]
  32. Kennison J. A. Transcriptional activation of Drosophila homeotic genes from distant regulatory elements. Trends Genet. 1993 Mar;9(3):75–79. doi: 10.1016/0168-9525(93)90227-9. [DOI] [PubMed] [Google Scholar]
  33. Kraut R., Levine M. Mutually repressive interactions between the gap genes giant and Krüppel define middle body regions of the Drosophila embryo. Development. 1991 Feb;111(2):611–621. doi: 10.1242/dev.111.2.611. [DOI] [PubMed] [Google Scholar]
  34. Kraut R., Levine M. Spatial regulation of the gap gene giant during Drosophila development. Development. 1991 Feb;111(2):601–609. doi: 10.1242/dev.111.2.601. [DOI] [PubMed] [Google Scholar]
  35. Lehmann R., Nüsslein-Volhard C. Abdominal segmentation, pole cell formation, and embryonic polarity require the localized activity of oskar, a maternal gene in Drosophila. Cell. 1986 Oct 10;47(1):141–152. doi: 10.1016/0092-8674(86)90375-2. [DOI] [PubMed] [Google Scholar]
  36. Lehmann R., Nüsslein-Volhard C. The maternal gene nanos has a central role in posterior pattern formation of the Drosophila embryo. Development. 1991 Jul;112(3):679–691. doi: 10.1242/dev.112.3.679. [DOI] [PubMed] [Google Scholar]
  37. Lehmann R., Nüsslein-Volhard C. hunchback, a gene required for segmentation of an anterior and posterior region of the Drosophila embryo. Dev Biol. 1987 Feb;119(2):402–417. doi: 10.1016/0012-1606(87)90045-5. [DOI] [PubMed] [Google Scholar]
  38. Moazed D., O'Farrell P. H. Maintenance of the engrailed expression pattern by Polycomb group genes in Drosophila. Development. 1992 Nov;116(3):805–810. doi: 10.1242/dev.116.3.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Mohler J., Eldon E. D., Pirrotta V. A novel spatial transcription pattern associated with the segmentation gene, giant, of Drosophila. EMBO J. 1989 May;8(5):1539–1548. doi: 10.1002/j.1460-2075.1989.tb03538.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Oliver B., Perrimon N., Mahowald A. P. The ovo locus is required for sex-specific germ line maintenance in Drosophila. Genes Dev. 1987 Nov;1(9):913–923. doi: 10.1101/gad.1.9.913. [DOI] [PubMed] [Google Scholar]
  41. Pankratz M. J., Busch M., Hoch M., Seifert E., Jäckle H. Spatial control of the gap gene knirps in the Drosophila embryo by posterior morphogen system. Science. 1992 Feb 21;255(5047):986–989. doi: 10.1126/science.1546296. [DOI] [PubMed] [Google Scholar]
  42. Paro R. Imprinting a determined state into the chromatin of Drosophila. Trends Genet. 1990 Dec;6(12):416–421. doi: 10.1016/0168-9525(90)90303-n. [DOI] [PubMed] [Google Scholar]
  43. Rastelli L., Chan C. S., Pirrotta V. Related chromosome binding sites for zeste, suppressors of zeste and Polycomb group proteins in Drosophila and their dependence on Enhancer of zeste function. EMBO J. 1993 Apr;12(4):1513–1522. doi: 10.1002/j.1460-2075.1993.tb05795.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Reinitz J., Levine M. Control of the initiation of homeotic gene expression by the gap genes giant and tailless in Drosophila. Dev Biol. 1990 Jul;140(1):57–72. doi: 10.1016/0012-1606(90)90053-l. [DOI] [PubMed] [Google Scholar]
  45. Rothe M., Nauber U., Jäckle H. Three hormone receptor-like Drosophila genes encode an identical DNA-binding finger. EMBO J. 1989 Oct;8(10):3087–3094. doi: 10.1002/j.1460-2075.1989.tb08460.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Schröder C., Tautz D., Seifert E., Jäckle H. Differential regulation of the two transcripts from the Drosophila gap segmentation gene hunchback. EMBO J. 1988 Sep;7(9):2881–2887. doi: 10.1002/j.1460-2075.1988.tb03145.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. 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]
  48. Simon M. A., Bowtell D. D., Dodson G. S., Laverty T. R., Rubin G. M. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell. 1991 Nov 15;67(4):701–716. doi: 10.1016/0092-8674(91)90065-7. [DOI] [PubMed] [Google Scholar]
  49. Sinclair D. A., Campbell R. B., Nicholls F., Slade E., Brock H. W. Genetic analysis of the additional sex combs locus of Drosophila melanogaster. Genetics. 1992 Apr;130(4):817–825. doi: 10.1093/genetics/130.4.817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Stearns T., Botstein D. Unlinked noncomplementation: isolation of new conditional-lethal mutations in each of the tubulin genes of Saccharomyces cerevisiae. Genetics. 1988 Jun;119(2):249–260. doi: 10.1093/genetics/119.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. 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]
  52. Struhl G. Differing strategies for organizing anterior and posterior body pattern in Drosophila embryos. Nature. 1989 Apr 27;338(6218):741–744. doi: 10.1038/338741a0. [DOI] [PubMed] [Google Scholar]
  53. Struhl G., Struhl K., Macdonald P. M. The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell. 1989 Jun 30;57(7):1259–1273. doi: 10.1016/0092-8674(89)90062-7. [DOI] [PubMed] [Google Scholar]
  54. Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma. 1989 Aug;98(2):81–85. doi: 10.1007/BF00291041. [DOI] [PubMed] [Google Scholar]
  55. Tautz D. Redundancies, development and the flow of information. Bioessays. 1992 Apr;14(4):263–266. doi: 10.1002/bies.950140410. [DOI] [PubMed] [Google Scholar]
  56. Wang C., Dickinson L. K., Lehmann R. Genetics of nanos localization in Drosophila. Dev Dyn. 1994 Feb;199(2):103–115. doi: 10.1002/aja.1001990204. [DOI] [PubMed] [Google Scholar]
  57. Wang C., Lehmann R. Nanos is the localized posterior determinant in Drosophila. Cell. 1991 Aug 23;66(4):637–647. doi: 10.1016/0092-8674(91)90110-k. [DOI] [PubMed] [Google Scholar]
  58. Wharton R. P., Struhl G. RNA regulatory elements mediate control of Drosophila body pattern by the posterior morphogen nanos. Cell. 1991 Nov 29;67(5):955–967. doi: 10.1016/0092-8674(91)90368-9. [DOI] [PubMed] [Google Scholar]
  59. Winston F., Carlson M. Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection. Trends Genet. 1992 Nov;8(11):387–391. doi: 10.1016/0168-9525(92)90300-s. [DOI] [PubMed] [Google Scholar]
  60. 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]
  61. Zink B., Paro R. In vivo binding pattern of a trans-regulator of homoeotic genes in Drosophila melanogaster. Nature. 1989 Feb 2;337(6206):468–471. doi: 10.1038/337468a0. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES