Abstract
The Polycomb (Pc) group of genes are required for maintenance of cell determination in Drosophila melanogaster. At least 11 Pc group genes have been described and there may be up to 40; all are required for normal regulation of homeotic genes, but as a group, their phenotypes are rather diverse. It has been suggested that the products of Pc group genes might be members of a heteromeric complex that acts to regulate the chromatin structure of target loci. We examined the phenotypes of adult flies heterozygous for every pairwise combination of Pc group genes in an attempt to subdivide the Pc group functionally. The results support the idea that Additional sex combs (Asx), Pc, Polycomblike (Pcl), Posterior sex combs (Psc), Sex combs on midleg (Scm), and Sex combs extra (Sce) have similar functions in some imaginal tissues. We show genetic interactions among extra sex combs (esc) and Asx, Enhancer of Pc, Pcl, Enhancer of zeste E(z), and super sex combs and reassess the idea that most Pc group genes function independently of esc. Most duplications of Pc group genes neither exhibit anterior transformations nor suppress the extra sex comb phenotype of Pc group mutations, suggesting that not all Pc group genes behave as predicted by the mass-action model. Surprisingly, duplications of E(z) enhance homeotic phenotypes of esc mutants. Flies with increasing doses of esc + exhibit anterior transformations, but these are not enhanced by mutations in trithorax group genes. The results are discussed with respect to current models of Pc group function.
Similar content being viewed by others
References
Adler PN, Charlton J, Brunk B (1989) Genetic interactions of the Suppressor 2 of zeste region genes. Dev Genet 10:249–260
Alberts B, Sternglanz R (1990) Chromatin contract to silence. Nature 344:193–194
Breen TR, Duncan IM (1986) Maternal expression of genes that regulate the bithorax complex of Drosophila melanogaster. Dev Biol 118:442–456
DeCamillis MA, Cheng N, Pierre D, Brock HW (1992) The polyhomeotic gene of Drosophila encodes a chromatin protein that shares polytene chromosome binding sites with Polycomb. Genes Dev 6:223–232
Denell RE (1978) Homoeosis in Drosophila. II. A genetic analysis of Polycomb. Genetics 84:277–289
Duncan IM (1982) Polycomblike: a gene that appears to be required for the normal expression of the bithorax and Antennapedia complexes of Drosophila melanogaster. Genetics 102:49–70
Duncan IM, Lewis EB (1982) Genetic control of body segment differentiation in Drosophila. Liss, New York
Dura J-M, Brock HW, Santamaria P (1985) Polyhomeotic: a gene in Drosophila melanogaster required for correct expression of segment identity. Mol Gen Genet 198:220–231
Dura J-M, Randsholt NB, Deatrick J, Erk I, Santamaria P, Freeman JD, Freeman SJ, Weddell D, Brock HW (1987) A complex genetic locus, polyhomeotic, is required for segmental specification and epidermal development in Drosophila melanogaster. Cell 51:829–839
Eissenberg JC, James TC, Foster-Hartnett DM, Hartnett T, Ngan V, Elgin SCR (1990) Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc Natl Acad Sci USA 87:9923–9927
Franke A, Decamillis M, Zink D, Cheng N, Brock HW, Paro R (1992) Polycomb and polyhomeotic are constituents of a multimeric protein complex in chromatia of Drosophila melanogaster. EMBO J 11:2941–2950
Gaunt SJ, Singh PB (1990) Homeogene expression patterns and chromosomal imprinting. Trends Genet 6:208–212
Girton JR, Jeon SH (1994) Novel embryonic and adult homeotic phenotypes are produced by pleiohomeotic mutations in Drosophila. Dev Biol 161:393–407
Glicksman MA, Brower DL (1988) Misregulation of homeotic gene expression in Drosophila larvae resulting from mutations at the extra sex combs locus. Dev Biol 126:219–227
Haynie JL (1983) The maternal and zygotic role of the gene Polycomb in embryonic determination in Drosophila melanogaster. Dev Biol 100:399–411
Ingham PW (1984) A gene that regulates the bithorax complex differently in larval and adult cells of Drosophila. Cell 37:815–823
Jones RS, Gelbart WM (1990) Genetic analysis of the Enhancer of zeste locus and its role in gene regulation in Drosophila melanogaster. Genetics 126:185–199
Jones RS, Gelbart WM (1993) The Drosophila Polycomb-group gene Enhancer of zeste shares a domain of sequence similarity with trithorax. Mol Cell Biol 13:6357–6366
Jürgens G (1985) A group of genes controlling the spatial expression of the bithorax complex in Drosophila. Nature 316:153–155
Kennison JA (1993) Transcriptional activation of Drosophila homeotic genes from distant regulatory elements. Trends Genet 9:75–79
Kennison JA, Russell MA (1987) Dosage-dependent modifiers of homeotic mutations in Drosophila melanogaster. Genetics 116:75–86
Kennison JA, Tamkun JW (1988) Dosage-dependent modifiers of Polycomb and Antennapedia mutations in Drosophila. Proc Natl Acad Sci USA 85:8136–8140
Landecker HL, Sinclair DAR, Brock HW (1994) A screen for enhancers of Polycomb and Polycomblike in Drosophila melanogaster. Dev Genet, in press
Lewis EB (1978) A gene complex controlling segmentation in Drosophila. Nature 276:565–570
Lindsley DL, Zimm GG (1992) The genome of Drosophila melanogaster. Academic Press, San Diego New York
Locke J, Kotarski MA, Tartof KD (1988) Dosage-dependent modifiers of position-effect variegation in Drosophila and a mass action model that explains their effect. Genetics 120:181–198
Martin EC, Adler PN (1993) The Polycomb group gene Posterior sex combs encodes a chromosomal protein. Development 117:641–655
McKeon J, Brock HW (1991) Interactions of the Polycomb group of genes with homeotic loci of Drosophila. Roux's Arch Dev Biol 199:387–396
Moazed D, O'Farrell PH (1992) Maintenance of the engrailed expression pattern by Polycomb group genes in Drosophila. Development 116:805–810
Paro R (1990) Imprinting a determined state into the chromatin of Drosophila. Trends Genet 6:416–421
Paro, R, Hogness DS (1991) The Polycomb protein shares a homologous domain with a heterochromatin-associated protein in Drosophila. Proc Natl Acad Sci USA 88:263–267
Peterson CL, Herskowitz I (1992) Characterization of the yeast SW1, SWI2, and SWI3 genes, which encode a global activator of transcription. Cell 68:573–583
Phillips MD, Shearn A (1990) Mutations in polycombeotic, a Drosophila Polycomb group gene, cause a wide range of maternal and zygotic phenotypes. Genetics 125:91–101
Puro J, Nygren J (1975) Mode of action of a homoeotic gene in Drosophila melanogaster. Hereditas 81:237–248
Rastelli L, Chan CS, Pirotta V (1993) Related chromosome binding sites for zeste, suppressor of zeste and Polycomb group protein and their dependence on Enhancer of zeste function. EMBO J 12:1513–1522
Reuter GM, Giarre M, Farah J, Gausz J, Spierer A, Spierer P (1990) Dependence of position-effect variegation in Drosophila on dose of a gene encoding an unusual zinc-finger protein. Nature 344:219–223
Sato T, Hayes PH, Denell RE (1984) Homeosis in Drosophila: maternal effect of the Enhancer of Polycomb locus and its interaction with Polycomb and related loci. Dev Genet 4:185–198
Simon J, Chiang A, Bender W (1992) Ten different Polycomb group genes are required for spatial control of the abd-A and Abd-B homeotic products. Development 114:493–505
Sinclair DAR, Campbell RB, Nicholls F, Slade E, Brock HW (1992) Genetic analysis of the Additional sex combs locus of Drosophila melanogaster. Genetics 130:817–825
Smouse D, Goodman CS, Mahowald A, Perrimon N (1988) Polyhomeotic: a gene required for the embryonic development of axon pathways in the central nervous system of Drosophila. Genes Dev 2:830–842
Struhl G (1981) A gene product required for correct initiation of segmental determination in Drosophila. Nature 293:36–41
Struhl G (1983) Role of the esc + gene product in ensuring the selective expression of segment-specific homeotic genes in Drosophila. J Embryol Exp Morphol 76:297–331
Struhl G, Akam ME (1985) Altered distribution of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J 4:3259–3264
Struhl G, Brower D (1982) Early role of the esc + gene product in the determination of segments in Drosophila. Cell 31:285–292
Wedeen C, Harding K, Levine M (1986) Spatial regulation of Antennapedia and bithorax gene expression by the Polycomb locus in Drosophila. Cell 44:739–748
Wu C-T, Jones RS, Lasko PF, Gelbart WM (1989) Homeosis and the interaction of zeste and white in Drosophila. Mol Gen Genet 218:559–564
Zink B, Paro R (1989) In vivo binding pattern of a trans-regulator of the homeotic genes in Drosophila melanogaster. Nature 337:468–471
Author information
Authors and Affiliations
Additional information
Communicated by J. Campos-Ortega
Rights and permissions
About this article
Cite this article
Campbell, R.B., Sinclair, D.A.R., Couling, M. et al. Genetic interactions and dosage effects of Polycomb group genes of Drosophila . Molec. Gen. Genet. 246, 291–300 (1995). https://doi.org/10.1007/BF00288601
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00288601