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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Adler PN, Charlton J, Brunk B (1989) Genetic interactions of theSuppressor 2 ofzeste region genes. Dev Genet 10:249–260
Atkinson KD (1985) Two recessive suppressors ofSaccharomyces cerevisiae CH01 that are unlinked but fall in the same complementation group. Genetics 111:1–6
Bienz M (1992) Molecular mechanisms of determination inDrosophila Curr Opin Cell Biol 4:955–961
Breen TR, Duncan IM (1986) Maternal expression of genes that regulate the bithorax complex ofDrosophila melanogaster. Dev Biol 118:442–456
Busturia A, Bienz M (1993) Silencers inAbdominal-B, a homeoticDrosophila gene. EMBO J 12:1415–1425
Busturia A, Morata G (1988) Ectopic expression of homeotic genes caused by the elimination of thePolycomb gene inDrosophila imaginal epidermis. Development 104:713–720
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
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
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
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
Dutcher SK, Gibbons W, Inwood WB (1988) A genetic analysis of suppressors of thePF10 mutation inChlamydomonas rheinhardtii Genetics 120:965–976
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
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
Fuller MT, Regan CL, Hays TS, Green LL (1989) Interacting genes identify proteins involved in microtubule formation inDrosophila. Cell Motil Cytoskel 14:128–135
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
Hochman B, Gloor H, Green MM (1964) Analysis of chromosome 4 inDrosophila melanogaster. I. Spontaneous and X-ray induced lethals. Genetica 35:109–126
Homyk T, Emerson CP (1988) Functional interactions between unlinked muscle genes with haploin sufficient regions of theDrosophila genome. Genetics 119:105–121
Ingham PW (1984) A gene that regulates the bithorax complex differently in larval and adult cells ofDrosophila. Cell 37:815–823
Jones RS, Gelbart WM (1990) Genetic analysis of theEnhancer of zeste locus and its role in gene regulation inDrosophila melanogaster. Genetics 126:185–199
Jurgens G (1985) A group of genes controlling the spatial expression of the bithorax complex inDrosophila. Nature 316:153–155
Kennison JA, Russell MA (1987) Dosage-dependent modifiers of homeotic mutations inDrosophila melanogaster. Genetics 116:75–86
Klein KK, Deppe CS (1985) Complementation and non-complementation among nonallelic mutations altering development inSchizophyllum commune. Genetics 109:333–339
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
Lewis EB (1978) A gene complex controlling segmentation inDrosophila. Nature 276:565–570
Lindsley DL, Zimm GG (1992) The genome ofDrosophila melanogaster. Academic Press, New York.
Martin EC, Adler PN (1993) ThePolycomb group genePosterior sex combs encodes a chromosomal protein. Development 117:641–655
McKeon J, Brock HW (1991) Interactions of thePolycomb group of genes with homeotic loci ofDrosophila. Roux's Arch Dev Biol 199:387–396
Moazed D, O'Farrell PH (1992) Maintenance of theengrailed expression pattern byPolycomb group genes inDrosophila. Development 116:805–810
Müller J, Bienz M (1991) Long range repression conferring boundaries ofUltrabithorax expression in theDrosophila embryo. EMBO J 10:3147–3156
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
Paro R, Zink B (1992) ThePolycomb gene is differentially regulated during oogenesis and embryogenesis ofDrosophila melanogaster. Mech Dev 40:37–46
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
Patel NH, Schafer B, Goodman CS, Holmgren R (1989b) The role of segment polarity genes duringDrosophila neurogenesis. Genes Dev 3:890–904
Phillips MD, Shearn A (1990) Mutations inpolycombeotic, aDrosophila Polycomb group gene, cause a wide range of maternal and zygotic phenotypes. Genetics 125:91–101
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
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
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
Rine J, Herskowitz I (1987) Four genes responsible for a position effect on expression fromHML andHMR inSaccharomyces cerevisiae. Genetics 116:9–22
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
Sinclair DR, Campbell RB, Nicholls F, Slade E, Brock HW (1992) Genetic analysis of theAdditional sex combs locus ofDrosophila 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 ofDrosophila. Genes Dev 2:830–842
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
Struhl G (1981) A gene product required for correct initiation of segmental determination inDrosophila. Nature 293:36–41
Struhl G (1982) Genes controlling segmental specification in theDrosophila thorax. Proc Natl Acad Sci USA 79:7380–7384
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
Struhl G, Akam ME (1985) Altered distribution ofUltrabithorax transcripts inextra sex combs mutant embryos ofDrosophila. EMBO J 4:3259–3264
Wedeen C, Harding K, Levine M (1986) Spatial regulation of Antennapedia and bithorax gene expression by thePolycomb locus inDrosophila. Cell 44:739–748
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
Zink B, Paro R (1989)In vivo binding pattern of a trans-regulator of the homeotic genes inDrosophila melanogaster. Nature 337:468–471
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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