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Characterization of a sex-influenced modifier of gene expression and suppressor of position-effect variegation inDrosophila

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Abstract

Modifier of white (Mow), a dominant transacting gene, has been identified through a mutagenic screen for second-site loci that alter the level of expression of thewhite eye color locus.Mow reduces the expression ofwhite in most developmental stages, but enhances its expression in the pupal stage, the time at which the major contribution to the adult phenotype is made. Tests with anAlcohol dehydrogenase promoter-white reporter and a series ofwhite truncation constructs have shown thatMow fails to affect the reporter; cis-regulatory mutations ofwhite also show no response, suggesting a requirement forwhite regulatory domains for interaction withMow. A quantitative analysis of steady-state transcript levels reveals that thewhite mRNA level decreases in the presence of one dose ofMow in larvae and adults, but the reduction is greater in females than males. Two other functionally related genes,brown andscarlet, also exhibit a similar sexually dimorphic alteration in expression, mediated byMow. In the mid-pupal stage, by contrast, the level ofwhite andbrown mRNA is increased byMow. In addition,Mow acts as a weak suppressor of position effect variegation (PEV). These observations suggest a connection between dosage modulation of gene expression and suppression of position-effect variegation.

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References

  1. Baker BS, Gorman M, Martin I (1994) Dosage compensation inDrosophila. Annu Rev Genet 28:491–521

  2. Belote JM, Lucchesi JC (1980)Male-specific lethal mutations ofDrosophila melanogaster. Genetics 96:165–186

  3. Bialogan S, Fauldenburg D, Renkawitz-Pohl D (1985) Characterization and developmental expression ofβ-tubulin genes inDrosophila melanogaster. EMBO J. 3:2543–2548

  4. Bickel S, Pirrotta V (1990) Self association of theDrosophila zeste protein is responsible for transvection effects. EMBO J 9:2959–2967

  5. Bingham PM, Chapman CH (1986) Evidence thatwhite blood is a novel type of temperature-sensitive mutation resulting from temperature-dependent effects of a transposon insertion on formation ofwhite transcripts. EMBO J 5:3343–3351

  6. Bingham PM, Judd BH (1981) A copy of thecopia transposable element is very tightly linked to thew a allele at thewhite locus ofD. melanogaster. Cell 25:705–711

  7. Bingham PM, Zachar Z (1985) Evidence that two mutations,w DZL andz 1, affecting synapsis-dependent genetic behaviour ofwhite are transcriptional regulatory mutations. Cell 40:819–825

  8. Birchler JA (1979) A study of enzyme activities in a dosage series of the long arm of chromosome 1 in maize. Genetics 92:1211–1229

  9. Birchler JA (1981) The genetic basis of dosage compensation ofAlcohol dehydrogenase-1 in maize. Genetics 97:625–637

  10. Birchler JA (1992) Expression of cis-regulatory mutations of thewhite locus in metafemales ofDrosophila melanogaster. Genet Res 59:11–18

  11. Birchler JA, Hiebert JC (1989) Interaction of theEnhancer of white-apricot with transposable element alleles at thewhite locus inDrosophila melanogaster. Genetics 122:129–138

  12. Birchler JA, Newton KJ (1981) Modulation of protein levels in chromosomal dosage series of maize: the biochemical basis of aneuploid syndromes. Genetics 99:247–266

  13. Birchler JA, Hiebert JC, Krietzmann M (1989a) Gene expression in adult metafemales ofDrosophila melanogaster. Genetics 122:869–879

  14. Birchler JA, Hiebert JC, Rabinow L (1989b) Interaction of themottler of white with transposable element alleles at thewhite locus inDrosophila melanogaster. Genes Dev 3:73–84

  15. Birchler JA, Hiebert JC, Paigen K (1990) Analysis of autosomal dosage compensation involving theAlcohol dehydrogenase locus inDrosophila melanogaster. Genetics 124:677–686

  16. Birchler JA, Bhadra U, Rabinow L, Linsk R, Nguyen-Huynh AT (1994)Weakener of white (Wow), a gene that modifies the expression of thewhite eye color locus and that suppresses position-effect variegation inDrosophila melanogaster. Genetics 137:1057–1070

  17. Carbonare BD, Gehring WJ (1985) Excision ofcopia element in a revertant of thewhite apricot mutation ofDrosophila melanogaster leaves behind one long terminal repeat. Mol Gen Genet 199:1–6

  18. Chen JD, Pirrotta V (1993) Multimerization of theDrosophila zeste protein is required for efficient DNA binding. EMBO J 12:2075–2083

  19. Collins M, Rubin GM (1982) Structure of theDrosophila mutable allelewhite crimson and itswhite ivory and wild-type derivatives. Cell 30:71–79

  20. Cox RA (1968) The use of guanidium chloride in the isolation of nucleic acids. Methods Enzymol 12:120–129

  21. Csink A, Linsk R, Birchler JA (1994a)Mosaic suppressor, a gene inDrosophila that affectscopia and acts as a recessive enhancer ofzeste. Genetics 136:573–583

  22. Csink A, Linsk R, Birchler JA (1994b) TheLighten up (Lip) gene ofDrosophila melanogaster, a modifier of retroelement expression, position effect variegation andwhite locus insertion alleles. Genetics 138:153–163

  23. Davis PS, Shen MW, Judd BH (1987) Asymmetrical pairings of transposons in and proximal to thewhite locus ofDrosophila account for four classes of regularly occurring exchange products. Proc Natl Acad Sci USA 84:174–178

  24. Davison D, Chapman C, Wedeen C, Bingham PM (1985) Genetic and physical studies of a portion of thewhite locus participating in transcriptional regulation and in synapsis-dependent interactions inDrosophila adult tissues. Genetics 110:479–494

  25. Devlin RH, Holm DG, Grigliatti TA (1982) Autosomal dosage compensation inDrosophila melanogaster strains trisomic for the left arm of chromosome 2. Proc Natl Acad Sci USA 79:1200–1204

  26. Devlin RH, Grigliatti TA, Holm DG (1984) Dosage compensation is transcriptionally regulated in autosomal trisomies ofDrosophila. Chromosoma 91:65–73

  27. Devlin RH, Holm DG, Grigliatti TA (1988) The influence of whole arm trisomy on gene expression inDrosophila. Genetics 118:87–101

  28. Dorn R, Krauss V, Reuter G, Saumweber H (1993) The enhancer of position-effect variegation ofDrosophila, E(var)3-93D, codes for a chromatin protein containing a conserved domain common to several transcriptional regulators. Proc Natl Acad Sci USA 90:11376–11380

  29. Dreesen TD, Johnson DH, Heinkoff S (1988) Thebrown protein ofDrosophila melanogaster is similar to thewhite protein and to components of active transport complexes. Mol Cell Biol 8:5206–5215

  30. Ganguly R, Ganguly N, Manning JE (1985) Isolation and characterization of theglucose-6-phosphate dehydrogenase gene ofDrosophila melanogaster. Gene 35:91–101

  31. Gehring WJ, Paro R (1980) Isolation of a hybrid plasmid with homologous sequences to a transposing element ofDrosophila. Cell 19:857–904

  32. Goldberg ML, Sheen JY, Gehring WL, Green MM (1983) Unequal crossing-over associated with asymmetrical synapsis between nomadic elements in theDrosophila melanogaster genome. Proc Natl Acad Sci USA 80:5017–5021

  33. Green MM (1963) Unequal crossing over and the genetical organization of thewhite locus ofDrosophila melanogaster. Z. Vererbungsl 94:200–214

  34. Guo M, Birchler JA (1994) Trans-acting dosage effects on the expression of model gene systems in maize aneuploids. Science 266:1999–2002

  35. Hayashi S, Ruddell A, Sinclair D, Grigliatti TA (1990) Chromosomal structure is altered by mutations that suppress or enhance position effect variegation. Chromosoma 99:391–400

  36. Hazelrigg T (1987) TheDrosophila white gene: a molecular update. Trends Genet 3:43–49

  37. Hazelrigg T, Levis R, Rubin GM (1984) Transformation ofwhite locus DNA inDrosophila: dosage compensation,zeste interaction and position effects. Cell 36:469–481

  38. Hearn MG, Hedrick A, Grigliatti TA, Wakimoto T (1991) The effect of modifiers of position-effect variegation on the variegation of heterochromatic genes ofDrosophila melanogaster. Genetics 128:785–797

  39. Henikoff S (1979) Position-effects and variegation enhancers in an autosomal region ofDrosophila melanogaster. Genetics 93:106–115

  40. Henikoff S (1990) Position-effect variegation after 60 years. Trends Genet 6:422–426

  41. Karess RE, Rubin GM (1982) A small tandem duplication is responsible for the unstablewhite ivory mutation inDrosophila. Cell 30:63–69

  42. Karpen G, Spradling AC (1990) Reduced DNA polytenization of a minichromosome region undergoing position-effect variegation inDrosophila. Cell 63:97–107

  43. Levis R, Hazelrigg T, Rubin GM (1985) Separable cis-acting control elements for expression of thewhite gene ofDrosophila. EMBO J 4:3489–3499

  44. Lewis EB, Bachar F (1968) Method of feeding ethyl methane sulfonate (EMS) toDrosophila males. Dros Inf Serv 43:193

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

  46. Locke JM, Kotarski A, Tartof KD (1988) Dosage-dependent modifiers of position effect variegation inDrosophila and a mass action model that explains their effect. Genetics 120:181–198

  47. Lucchesi JC, Skripsky T (1981) The link between dosage compensation and sex differentiation inDrosophila melanogaster. Chromosoma 82:217–227

  48. Mansukhani A, Crickmore A, Sherwood PW, Sneath BJ, Goldberg ML (1988) DNA-binding properties of theDrosophila melanogaster zeste gene product. Mol Cell Biol 615–623

  49. Mount SM, Green MM, Rubin GM (1988) Partial revertants of the transposable element-associated suppressible allelewhite apricot inDrosophila melanogaster. Genetics 118:221–234

  50. O'Hare K, Levis R, Rubin GM (1983) Transcription of thewhite locus inDrosophila melanogaster. Proc Natl Acad Sci USA 80:6917–6921

  51. O'Hare K, Murphy C, Levis R, Rubin GM (1984) DNA sequence of thewhite locus ofDrosophila melanogaster. J Mol Biol 180:437–455

  52. O'Hare K, Alley MRK, Cullingford TE, Driver A, Sanderson MJ (1991) DNA sequence of theDoc retroposon in thewhite-one mutant ofDrosophila melanogaster and of secondary insertions in the phenotypically altered derivativeswhite-honey andwhite-eosin. Mol Gen Genet 225:17–24

  53. Qian S, Pirrotta V (1995) Dosage compensation of theDrosophila white gene requires both theX chromosome environment and multiple intragenic elements. Genetics 139:733–744

  54. Rabinow L, Nguyen-Huynh AT, Birchler JA (1991) A trans-acting regulatory gene that inversely affects the expression of thewhite, brown andscarlet loci inDrosophila. Genetics 129:463–480

  55. Reichert GH (1986) Two-dimensional gel analysis of proteins from mouse fetuses with trisomy 19 after DEAE-Sepharose chromatography. Genet Res 47:193–197

  56. Reuter G, Wolf I (1981) Isolation of dominant suppressor mutations for position-effect variegation inDrosophila melanogaster. Mol Gen Genet 182:516–519

  57. Reuter G, Dorn R, Wüstman G, Friede B, Rauh G (1986) Third chromosome suppressor of position-effect variegation loci inDrosophila melanogaster. Mol Gen Genet 202:481–487

  58. Reuter G, Gausz J, Gyurkovics H, Friede B, Bang R, Spierer A, Hall LMC, Spierer P (1987) Modifiers of position effect variegation in the region from 86C to 88B of theDrosophila melanogaster third chromosome. Mol Gen Genet 210:429–436

  59. Reuter G, Giarre M, Farah J, Gausz J, Spierer A, Spierer P (1990) Dependence of position-effect variegation inDrosophila on dose of a gene encoding an unusual zinc-finger protein. Nature 344:219–223

  60. Sabl J, Birchler JA (1993) Dosage dependent modifiers ofwhite alleles inDrosophila melanogaster. Genet Res 62:15–22

  61. Sang HM, Pelisson A, Bucheton A, Finnegan DJ (1984) Molecular lesions associated withwhite gene mutations induced by I-R hybrid dysgenesis inDrosophila melanogaster. EMBO J 3:3079–3085

  62. Scott MJ, Lucchesi JC (1991) Structure and expression of theDrosophila melanogaster gene encoding 6-phosphogluconate dehydrogenase. Gene 109:177–183

  63. Sinclair DAR, Mottus RC, Grigliatti TA (1983) Genes which suppress position-effect variegation inDrosophila melanogaster are clustered. Mol Gen Genet 191:326–333

  64. Talbert PB, LeCiel CDS, Henikoff S (1994) Modification of theDrosophila heterochromatic mutationbrown Dominant by linkage alterations. Genetics 136:559–571

  65. Tearle RG, Belote JM, McKeown M, Baker BS, Howells AJ (1989) Cloning and characterization of thescarlet gene ofDrosophila melanogaster. Genetics 122:595–606

  66. Tschiersch B, Hofmann A, Krauss V, Dorn R, Korge G, Reuter G (1994) The protein encoded by theDrosophila position-effect variegation suppressor geneSu(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J 13:3822–3831

  67. Wüstman G, Szidonya J, Taubert H, Reuter G (1989) The genetics of position effect variegation-modifying loci inDrosophila melanogaster. Mol Gen Genet 217:520–527

  68. Zachar Z, Bingham PM (1982) Regulation ofwhite locus expression: the structure of mutant alleles at thewhite locus inDrosophila melanogaster. Cell 30:529–541

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Correspondence to Utpal Bhadra.

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Communicated by J. A. Campos-Ortega

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Bhadra, U., Birchler, J.A. Characterization of a sex-influenced modifier of gene expression and suppressor of position-effect variegation inDrosophila . Molec. Gen. Genet. 250, 601–613 (1996). https://doi.org/10.1007/BF02174448

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Key words

  • Sex-influenced modifier
  • Position effect variegation
  • Dosage effects
  • Drosophila melanogaster