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The multi sex combs gene of Drosophila melanogaster is required for proliferation of the germline

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Abstract

We present a genetic analysis showing that the Drosophila melanogaster gene multi sex combs (mxc; Santamaria and Randsholt 1995) is needed for proliferation of the germline. Fertility is the feature most easily affected by weak hypomorphic mutations of this very pleiotropic locus. Pole cell formation and early steps of gonadogenesis conform to the wild-type in embryos devoid of zygotic mxc + product. mxc mutant gonad phenotypes and homozygous mxc germline clones suggest a role for mxc + in control of germ cell proliferation during the larval stages. mxc + requirement is germ cell autonomous and specific in females, whilst in males mxc + product is also needed in somatic cells of the gonads. Although mxc can be classified among the Polycomb group (Pc-G) of genes, negative trans-regulators of the ANT-C and BX-C gene complexes, germline requirement for mxc appears independent of a need for other Pc-C gene products, and mxc gonad phenotypes are different from those induced by mutations in BX-C genes. We discuss the possible functions of the mxc + product which helps to maintain homeotic genes repressed and prevents premature larval haemocyte differentiation and neoplasic overgrowth, but promotes growth and differentiation of male and female gonads.

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References

  • Audit-Lamour C, Busson D (1981) Oogenesis defects in the ecd-1 mutant of Drosophila melanogaster, deficient in ecdysteroid at high temperature. J Insect Physiol 27:829–837

    Google Scholar 

  • Binari R, Perrimon N (1994) Stripe-specific regulation of pair-rule genes by hopscotch, a putative Jak family tyrosine kinase in Drosophila. Genes Dev 8:300–312

    Google Scholar 

  • Bodenstein D (1965) The post embryonic development of Drosophila. In: Demerec M (ed) Biology of Drosophila. Hafner Publishing Company, New York, pp 302–313

    Google Scholar 

  • Botas J (1985) Análisis genético de la Regulación de los complejos Bithorax y Antennapedia de la Drosophila melanogaster. Thesis of Universidad Autónoma de Madrid, Spain

  • Campos-Ortega JA, Hartenstein V (1985) The embryonic development of Drosophila melanogaster. Springer, Berlin Heidelberg New York, pp 98–103

    Google Scholar 

  • Castrillon DH, Wasserman SA (1994) diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the product of the limb deformity gene. Development 120:3367–3377

    Google Scholar 

  • Castrillon DH, Gönczy P, Alexander S, Rawson R, Eberhart CG, Viswanathan S, DiNardo S, Wasserman SA (1993) Towards a molecular genetic analysis of spermatogenesis in Drosophila melanogaster. Characterization of male-sterile mutants generated by single P-element mutagenesis. Genetics 135:489–505

    Google Scholar 

  • Cumberledge S, Szabad J, Sakonju S (1992) Gonadal formation and development requires the abd-A domain of the bithorax complex in Drosophila melanogaster. Development 115:395–402

    Google Scholar 

  • Dübendorfer K, Nöthiger R (1982) A clonal analysis of cell lineage and growth in the male and female genital disc of Drosophila melanogaster. Roux's Arch Dev Biol 191:42–55

    Google Scholar 

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

    Google Scholar 

  • Dura J-M, Deatrick J, Randsholt NB, Brock HW Santamaria P (1988) Maternal and zygotic requirement for the polyhomeotic complex genetic locus in Drosophila. Roux's Arch Dev Biol 197:239–246

    Google Scholar 

  • Epper F, Nöthinger R (1982) Genetic and developmental evidence for a repressed genital primordium in Drosophila melanogaster. Dev Biol 94:163–175

    Google Scholar 

  • Fuller MT (1993) Spermatogenesis In: Bate M, Martinez Arias A (eds) The development of Drosophila melanogaster, vol 1. Cold Spring Harbor Laboratory Press, pp 72–147

  • Gateff E (1978) Malignant neoplasms of genetic origin in Drosophila melanogaster. Science 200:1448–1459

    Google Scholar 

  • Gateff E, Mechler BM (1989) Tumor-suppressor genes of Drosophila melanogaster (Critical reviews in oncogenesis, vol 1) CRC Press, pp 221–245

  • Girton JR, Jeon SH (1994) Novel embryonic and adult homeotic phenotypes are produced by pleiohomeotic mutations in Drosophila. Dev Biol 161:393–407

    Google Scholar 

  • Harrison DA, Binari R, Stines Naheini T, Gilman M, Perrimon N (1995) Activation of a Drosophila Janus kinase (JAK) causes hematopoietic neoplasis and developmental defects. EMBO J 14:2857–2865

    Google Scholar 

  • Jaglarz MK, Howard KR (1994) Primordial germ cell migration in Drosophila melanogaster is controlled by somatic tissue. Development 120:83–89

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • Kemphues KJ, Kaufman TC, Raff RA, Raff EC (1982) The testis-specific β-tubulin subunit in Drosophila melanogaster has multiple functions in spermatogenesis. Cell 31:655–670

    Google Scholar 

  • King RC (1970) Ovarian development in Drosophila melanogaster. Academic Press, New York

    Google Scholar 

  • Lasko PE Ashburner M (1990) Posterior localization of vasa protein correlates with, but is not sufficient for, pole cell development. Genes Dev 4:905–921

    Google Scholar 

  • Lehman R, Nüsslein-Volhard C (1986) Abdominal segmentation, pole cell formation, and embryonic polarity require the localized activity of oskar, a maternal gene in Drosophila. Cell 47:141–152

    Google Scholar 

  • Lindsley DL, Zimm GG (1992) The genome of Drosophila melanogaster. Academic Press, Harcourt Brace Jovanovich, San Diego

    Google Scholar 

  • Mansfield E, Hersperger E, Biggs J, Shearn A (1994) Genetic and molecular analysis of hyperplastic discs, a gene whose product is required for regulation of cell proliferation in Drosophila melanogaster imaginal discs and germ cells. Dev Biol 165:507–526

    Google Scholar 

  • Martin P, Martin A, Shearn A (1977) Studies of 1(3)c43hs1 a polyphasic, temperature-sensitive mutant of Drosophila melanogaster with a variety of imaginal disc defects. Dev Biol 55:213–232

    Google Scholar 

  • McKeon J, Brock HW (1991) Interactions of the Polycombgroup of genes with homeotic loci of Drosophila. Roux's Arch Dev Biol 199:387–391

    Google Scholar 

  • McKeon J, Slade E, Sinclair DAR, Cheng N, Couling M, Brock HW (1994) Mutations in some Polycomb group genes of Drosophila interfere with regulation of segmentation genes. Mol Gen Genet 244:474–483

    Google Scholar 

  • Mével-Ninio M, Terracol R, Salles C, Vincent A, Payre F (1995) ovo, a Drosophila gene required for ovarian development, is specifically expressed in the germline and shares most of its coding sequences with shavenbaby, a gene involved in embryo patterning. Mech Dev 49:83–95

    Google Scholar 

  • Moazed D, O'Farrell PH (1992) Maintenance of the engrailed expression pattern by Polycomb group genes in Drosophila. Development 116:805–810

    Google Scholar 

  • Nishida Y, Hata M, Ayaki T, Ryo H, Yamagata M, Shimizu K, Nishizuka Y (1988) Proliferation of both somatic and germ cells is affected in the Drosophila mutants of raf proto-oncogene. EMBO J 7:775–781

    Google Scholar 

  • Oliver B, Perrimon N, Mahowald AP (1987) The ovo locus is required for sex-specific germ line maintenance in Drosophila. Genes Dev 1:913–923

    Google Scholar 

  • Paro R (1991) Imprinting a determined state into the chromatin of Drosophila. Trends Genet 6:416–421

    Google Scholar 

  • Paro R, Hogness DS (1991) The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc Nail Acad Sci USA 88:263–267

    Google Scholar 

  • Pelegri F, Lehmann R (1994) A role of Polycomb group genes in regulation of gap gene expression in Drosophila. Genetics 136:1341–1353

    Google Scholar 

  • Perrimon N (1984) Clonal analysis of dominant female-sterile, germline-dependent mutations in Drosophila melanogaster. Genetics 108:927–939

    Google Scholar 

  • Perrimon N, Mahowald AP (1986) 1(1)hopscotch, a larval-pupal zygotic lethal with a specific maternal effect on segmentation in Drosophila. Dev Biol 118:28–41

    Google Scholar 

  • 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

    Google Scholar 

  • Sánchez-Herrero E, Crosby MA (1988) The Abdominal-B gene of Drosophila melanogaster: overlapping transcripts exhibit two different spatial distributions. EMBO J 7:2163–2173

    Google Scholar 

  • Santamaría P (1986) Injecting eggs. In: Roberts DB (ed) Drosophila, a practical approach. IRL Press, Oxford, pp 159–173

    Google Scholar 

  • Santamaría P (1993) Evolution and aggregulates: role of the Polycomb-group genes of Drosophila. CR Acad Sci Paris Life Sci 316:1200–1206

    Google Scholar 

  • Santamaría P, Randsholt NB (1995) Characterization of a region of the X chromosome of Drosophila including multi sex combs (mxc), a Polycomb group gene which also functions as a tumor suppressor. Mol Gen Genet 246:282–290

    Google Scholar 

  • Santamaría P, Deatrick J, Randsholt NB (1989) Pattern triplications following genetic ablation on the wing of Drosophila: effect of eliminating the polyhomeotic gene. Roux's Arch Dev Biol 198:65–77

    Google Scholar 

  • Schloßherr J, Eggert H, Paro R, Cremer S, Jack RS (1994) Gene inactivation in Drosophila mediated by the gene product or by position-effect variegation does not involve major changes in the accesibility of the chromatin fibre. Mol Gen Genet 243: 453–462

    Google Scholar 

  • Schüpbach T, Wieschaus E (1991) Female sterile mutations on the second chromosome of Drosophila melanogaster. II Mutations blocking oogenesis or altering egg morphology. Genetics 129: 1119–1136

    Google Scholar 

  • Simon J, Chiang A, Bender W (1992) Ten different Polycomb group genes are required for spatial control of the abdA and AbdB homeotic products. Development 114:493–505

    Google Scholar 

  • Spradling AC (1993) Oogenesis. In: Bate M, Martinez Arias A (eds) The development of Drosophila melanogaster, vol 1. Cold Spring Harbor Laboratory Press, pp 1–70

  • St Johnston D (1993) Pole plasm and the posterior group genes. In: Bate M, Martinez Arias A (eds) The development of Drosophila melanogaster, vol 1. Cold Spring Harbor Laboratory Press, pp 325–363

  • Verheyen EM, Cooley L (1994) Profilin mutations disrupt multiple actin-dependent processes during Drosophila development. Development 120:717–728

    Google Scholar 

  • Warrior R (1994) Primordial germ cell migration and the assembly of the Drosophila embryonic gonad. Dev Biol 166:180–194

    Google Scholar 

  • Watson KL, Konrad KD, Woods DE Bryant P (1992) Drosophila homolog of the human S6 ribosomal protein is required for tumor suppression in the hematopoietic system. Proc Natl Acad Sci USA 89:11302–11306

    Google Scholar 

  • Watson KL, Justice RW Bryant PJ (1994) Drosophila in cancer research: the first fifty tumor supressor genes. J Cell Sci S18:19–33

    Google Scholar 

  • Wu C-T, Jones RS, Lasko PE Gelbart WM (1989) Homeosis and the interaction of zeste and white in Drosophila. Mol Gen Genet 218:559–564

    Google Scholar 

Download references

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Authors and Affiliations

  1. Département Génome et Développement, Centre de Génétique Moléculaire du CNRS, F-91198, Gif sur Yvette Cedex, France

    France Docquier, Olivier Saget, Françoise Forquignon, Neel B. Randsholt & Pedro Santamaria

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  1. France Docquier
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  2. Olivier Saget
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  3. Françoise Forquignon
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  4. Neel B. Randsholt
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  5. Pedro Santamaria
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F.D. and O.S. should be considered as equal first authors

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Docquier, F., Saget, O., Forquignon, F. et al. The multi sex combs gene of Drosophila melanogaster is required for proliferation of the germline. Roux's Arch Dev Biol 205, 203–214 (1996). https://doi.org/10.1007/BF00365798

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