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Mutations in somePolycomb group genes ofDrosophila interfere with regulation of segmentation genes

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Abstract

Mutations in severalPolycomb (Pc) group genes cause maternal-effect or zygotic segmentation defects, suggesting thatPc group genes may regulate the segmentation genes ofDrosophila. We show that individuals doubly heterozygous for mutations inpolyhomeotic and six otherPc group genes show gap, pair rule, and segment polarity segmentation defects. We examined double heterozygous combinations ofPc group and segmentation mutations for enhancement of adult and embryonic segmentation defects.Posterior sex combs andpolyhomeotic interact withKrüppel 2 and enhance embryonic phenotypes ofhunchback andknirps, andpolyhomeotic enhanceseven-skipped. Surprisingly, flies carrying duplications ofextra sex combs (esc), that were heterozygous for mutations ofeven-skipped (eve), were extremely subvital. Embryos and surviving adults of this genotype showed strong segmentation defects in even-numbered segments. Antibody studies confirm that expression ofeve is suppressed by duplications ofesc. However,esc duplications have no effect on other gap or pair rule genes tested. To our knowledge, this is only the second triplo-abnormal phenotype associated withPc group genes. Duplications of nine otherPc group genes have no detectable effect oneve. Expression ofengrailed (en) was abnormal in the central nervous systems of mostPc group mutants. These results support a role forPc genes in regulation of some segmentation genes, and suggest thatesc may act differently from otherPc group genes.

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References

  • Adler PN, Charlton J, Brunk B (1989) Genetic interactions of theSuppressor 2 ofzeste region genes. Dev Genet 10:249–260

    Google Scholar 

  • Atkinson KD (1985) Two recessive suppressors ofSaccharomyces cerevisiae CH01 that are unlinked but fall in the same complementation group. Genetics 111:1–6

    Google Scholar 

  • Bienz M (1992) Molecular mechanisms of determination inDrosophila Curr Opin Cell Biol 4:955–961

    Google Scholar 

  • Breen TR, Duncan IM (1986) Maternal expression of genes that regulate the bithorax complex ofDrosophila melanogaster. Dev Biol 118:442–456

    Google Scholar 

  • Busturia A, Bienz M (1993) Silencers inAbdominal-B, a homeoticDrosophila gene. EMBO J 12:1415–1425

    Google Scholar 

  • Busturia A, Morata G (1988) Ectopic expression of homeotic genes caused by the elimination of thePolycomb gene inDrosophila imaginal epidermis. Development 104:713–720

    Google Scholar 

  • DeCamillis MA, Cheng N, Pierre D, Brock HW (1992) Thepolyhomeotic gene ofDrosophila encodes a chromatin protein that shares polytene chromosome binding sites withPolycomb. Genes Dev 6:223–232

    Google Scholar 

  • Duncan IM (1982)Polycomblike: a gene that appears to be required for the normal expression of the bithorax and Antennapedia complexes ofDrosophila melanogaster. Genetics 102:49–70

    Google Scholar 

  • Dura J-M, Ingham PW (1988) Tissue- and stage-specific control of homeotic and segmentation gene expression inDrosophila embryos by thepolyhomeotic gene. Development 103:733–741

    Google Scholar 

  • Dura J-M, Brock HW, Santamaria P (1985)Polyhomeotic: a gene inDrosophila melanogaster required for correct expression of segment identity. Mol Gen Genet 198:220–231

    Google Scholar 

  • Dutcher SK, Gibbons W, Inwood WB (1988) A genetic analysis of suppressors of thePF10 mutation inChlamydomonas rheinhardtii Genetics 120:965–976

    Google Scholar 

  • Franke A, DeCamillis MA, Zink D, Cheng N, H.W. Brock, Paro R (1992)Polycomb andpolyhomeotic are constituents of a multimeric protein complex in chromatin ofDrosophila melanogaster. EMBO J 11:2941–2950

    Google Scholar 

  • Fuller MT, Caulton JH, Hutchens JA, Kaufman TC, Raff EC (1987) Genetic analysis of microtubule structure: a beta-tubulin mutation causes the formation of aberrant microtubulesin vivo andin vitro. J Cell Biol 104:385–394

    Google Scholar 

  • Fuller MT, Regan CL, Hays TS, Green LL (1989) Interacting genes identify proteins involved in microtubule formation inDrosophila. Cell Motil Cytoskel 14:128–135

    Google Scholar 

  • Hays TS, Denting R, Robertson B, Prout M, Fuller MT (1989) Interacting proteins identified by genetic interactions: a missense mutation in alpha-tubulin fails to complement alleles of the testis-specific beta-tubulin gene ofDrosophila melanogaster. Mol Cell Biol 9:875–884

    Google Scholar 

  • Hochman B, Gloor H, Green MM (1964) Analysis of chromosome 4 inDrosophila melanogaster. I. Spontaneous and X-ray induced lethals. Genetica 35:109–126

    Google Scholar 

  • Homyk T, Emerson CP (1988) Functional interactions between unlinked muscle genes with haploin sufficient regions of theDrosophila genome. Genetics 119:105–121

    Google Scholar 

  • Ingham PW (1984) A gene that regulates the bithorax complex differently in larval and adult cells ofDrosophila. Cell 37:815–823

    Google Scholar 

  • Jones RS, Gelbart WM (1990) Genetic analysis of theEnhancer of zeste locus and its role in gene regulation inDrosophila melanogaster. Genetics 126:185–199

    Google Scholar 

  • Jurgens G (1985) A group of genes controlling the spatial expression of the bithorax complex inDrosophila. Nature 316:153–155

    Google Scholar 

  • Kennison JA, Russell MA (1987) Dosage-dependent modifiers of homeotic mutations inDrosophila melanogaster. Genetics 116:75–86

    Google Scholar 

  • Klein KK, Deppe CS (1985) Complementation and non-complementation among nonallelic mutations altering development inSchizophyllum commune. Genetics 109:333–339

    Google Scholar 

  • Kusch M, Edgar RS (1986) Genetic studies of unusual loci that affect body shape of the nematodeCaenorhabditis elegans and may code for structural proteins. Genetics 113:621–639

    Google Scholar 

  • Lewis EB (1978) A gene complex controlling segmentation inDrosophila. Nature 276:565–570

    Google Scholar 

  • Lindsley DL, Zimm GG (1992) The genome ofDrosophila melanogaster. Academic Press, New York.

    Google Scholar 

  • Martin EC, Adler PN (1993) ThePolycomb group genePosterior sex combs encodes a chromosomal protein. Development 117:641–655

    Google Scholar 

  • McKeon J, Brock HW (1991) Interactions of thePolycomb group of genes with homeotic loci ofDrosophila. Roux's Arch Dev Biol 199:387–396

    Google Scholar 

  • Moazed D, O'Farrell PH (1992) Maintenance of theengrailed expression pattern byPolycomb group genes inDrosophila. Development 116:805–810

    Google Scholar 

  • Müller J, Bienz M (1991) Long range repression conferring boundaries ofUltrabithorax expression in theDrosophila embryo. EMBO J 10:3147–3156

    Google Scholar 

  • Paro R, Hogness DS (1991) ThePolycomb protein shares a homologous domain with a heterochromatin-associated protein inDrosophila. Proc Natl Acad Sci USA 88:263–267

    Google Scholar 

  • Paro R, Zink B (1992) ThePolycomb gene is differentially regulated during oogenesis and embryogenesis ofDrosophila melanogaster. Mech Dev 40:37–46

    Google Scholar 

  • Patel NH, Martin-Blanco E, Coleman KG, Poole SJ, Ellis MC, Kornberg TB, Goodman CS (1989a) Expression ofengrailed proteins in arthropods, annelids, and chordates. Cell 58:955–968

    Google Scholar 

  • Patel NH, Schafer B, Goodman CS, Holmgren R (1989b) The role of segment polarity genes duringDrosophila neurogenesis. Genes Dev 3:890–904

    Google Scholar 

  • Phillips MD, Shearn A (1990) Mutations inpolycombeotic, aDrosophila Polycomb group gene, cause a wide range of maternal and zygotic phenotypes. Genetics 125:91–101

    Google Scholar 

  • Preiss A, Rosenberg UB, Kienlin A, Seifert E, Jackle H (1985) Molecular genetics ofKrüppel, a gene required for segmentation of theDrosophila embryo. Nature 313:27–32

    Google Scholar 

  • Rastelli L, Chan CS, Pirotta V (1993) Related chromosome binding sites forzeste, suppressor ofzeste andPolycomb group protein and their dependence onEnhancer of zeste function. EMBO J 12:1513–1522

    Google Scholar 

  • Regan CL, Fuller MT (1988) Interacting genes that affect microtubule function: thene2 allele of thehaywire locus fails to complement mutations in the testis-specific β-tubulin ofDrosophila. Genes Dev 2:82–92

    Google Scholar 

  • Rine J, Herskowitz I (1987) Four genes responsible for a position effect on expression fromHML andHMR inSaccharomyces cerevisiae. Genetics 116:9–22

    Google Scholar 

  • Simon J, Chiang A, Bender W (1992) Ten differentPolycomb group genes are required for spatial control of theAbd-A andAbd-B homeotic products. Development 114:493–505

    Google Scholar 

  • Sinclair DR, Campbell RB, Nicholls F, Slade E, Brock HW (1992) Genetic analysis of theAdditional sex combs locus ofDrosophila melanogaster. Genetics 130:817–825

    Google Scholar 

  • 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 ofDrosophila. Genes Dev 2:830–842

    Google Scholar 

  • Stearns T, Botstein D (1988) Unlinked non-complementation: isolation of new conditional lethal mutations in each of the tubulin genes ofSaccharomyces cerevisiae. Genetics 119:249–260

    Google Scholar 

  • Struhl G (1981) A gene product required for correct initiation of segmental determination inDrosophila. Nature 293:36–41

    Google Scholar 

  • Struhl G (1982) Genes controlling segmental specification in theDrosophila thorax. Proc Natl Acad Sci USA 79:7380–7384

    Google Scholar 

  • Struhl G (1983) Role of theesc + gene product in ensuring the selective expression of segment-specific homeotic genes inDrosophila. J Embryol Exp Morphol 76:297–331

    Google Scholar 

  • Struhl G, Akam ME (1985) Altered distribution ofUltrabithorax transcripts inextra sex combs mutant embryos ofDrosophila. EMBO J 4:3259–3264

    Google Scholar 

  • Wedeen C, Harding K, Levine M (1986) Spatial regulation of Antennapedia and bithorax gene expression by thePolycomb locus inDrosophila. Cell 44:739–748

    Google Scholar 

  • Zhang C-C, Beinz M (1992) Segmental determination inDrosophila conferred byhunchback, a repressor of the homeotic geneUltrabithorax. Proc Natl Acad Sci USA 89:7511–7515

    Google Scholar 

  • Zink B, Paro R (1989)In vivo binding pattern of a trans-regulator of the homeotic genes inDrosophila melanogaster. Nature 337:468–471

    Google Scholar 

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Communicated by J. Campos-Ortega

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McKeon, J., Slade, E., Sinclair, D.A.R. et al. Mutations in somePolycomb group genes ofDrosophila interfere with regulation of segmentation genes. Molec. Gen. Genet. 244, 474–483 (1994). https://doi.org/10.1007/BF00583898

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  • DOI: https://doi.org/10.1007/BF00583898

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