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Genetics. Dec 2000; 156(4): 1853–1865.
PMCID: PMC1461397

Evolution of dosage compensation in Diptera: the gene maleless implements dosage compensation in Drosophila (Brachycera suborder) but its homolog in Sciara (Nematocera suborder) appears to play no role in dosage compensation.

Abstract

In Drosophila melanogaster and in Sciara ocellaris dosage compensation occurs by hypertranscription of the single male X chromosome. This article reports the cloning and characterization in S. ocellaris of the gene homologous to maleless (mle) of D. melanogaster, which implements dosage compensation. The Sciara mle gene produces a single transcript, encoding a helicase, which is present in both male and female larvae and adults and in testes and ovaries. Both Sciara and Drosophila MLE proteins are highly conserved. The affinity-purified antibody to D. melanogaster MLE recognizes the S. ocellaris MLE protein. In contrast to Drosophila polytene chromosomes, where MLE is preferentially associated with the male X chromosome, in Sciara MLE is found associated with all chromosomes. Anti-MLE staining of Drosophila postblastoderm male embryos revealed a single nuclear dot, whereas Sciara male and female embryos present multiple intranuclear staining spots. This expression pattern in Sciara is also observed before blastoderm stage, when dosage compensation is not yet set up. The affinity-purified antibodies against D. melanogaster MSL1, MSL3, and MOF proteins involved in dosage compensation also revealed no differences in the staining pattern between the X chromosome and the autosomes in both Sciara males and females. These results lead us to propose that different proteins in Drosophila and Sciara would implement dosage compensation.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Akhtar A, Becker PB. Activation of transcription through histone H4 acetylation by MOF, an acetyltransferase essential for dosage compensation in Drosophila. Mol Cell. 2000 Feb;5(2):367–375. [PubMed]
  • Amrein H, Axel R. Genes expressed in neurons of adult male Drosophila. Cell. 1997 Feb 21;88(4):459–469. [PubMed]
  • Bachiller D, Sánchez L. Mutations affecting dosage compensation in Drosophila melanogaster: effects in the germline. Dev Biol. 1986 Dec;118(2):379–384. [PubMed]
  • Bashaw GJ, Baker BS. Dosage compensation and chromatin structure in Drosophila. Curr Opin Genet Dev. 1996 Aug;6(4):496–501. [PubMed]
  • Bashaw GJ, Baker BS. The regulation of the Drosophila msl-2 gene reveals a function for Sex-lethal in translational control. Cell. 1997 May 30;89(5):789–798. [PubMed]
  • Belote JM, Lucchesi JC. Male-specific lethal mutations of Drosophila melanogaster. Genetics. 1980 Sep;96(1):165–186. [PMC free article] [PubMed]
  • Bone JR, Kuroda MI. Dosage compensation regulatory proteins and the evolution of sex chromosomes in Drosophila. Genetics. 1996 Oct;144(2):705–713. [PMC free article] [PubMed]
  • Brockdorff N. The role of Xist in X-inactivation. Curr Opin Genet Dev. 1998 Jun;8(3):328–333. [PubMed]
  • Brockdorff N, Ashworth A, Kay GF, Cooper P, Smith S, McCabe VM, Norris DP, Penny GD, Patel D, Rastan S. Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome. Nature. 1991 May 23;351(6324):329–331. [PubMed]
  • Brunak S, Engelbrecht J, Knudsen S. Prediction of human mRNA donor and acceptor sites from the DNA sequence. J Mol Biol. 1991 Jul 5;220(1):49–65. [PubMed]
  • Burgess S, Couto JR, Guthrie C. A putative ATP binding protein influences the fidelity of branchpoint recognition in yeast splicing. Cell. 1990 Mar 9;60(5):705–717. [PubMed]
  • Campuzano S, Balcells L, Villares R, Carramolino L, García-Alonso L, Modolell J. Excess function hairy-wing mutations caused by gypsy and copia insertions within structural genes of the achaete-scute locus of Drosophila. Cell. 1986 Jan 31;44(2):303–312. [PubMed]
  • Kelley RL, Wang J, Bell L, Kuroda MI. Sex lethal controls dosage compensation in Drosophila by a non-splicing mechanism. Nature. 1997 May 8;387(6629):195–199. [PubMed]
  • Kelley RL, Meller VH, Gordadze PR, Roman G, Davis RL, Kuroda MI. Epigenetic spreading of the Drosophila dosage compensation complex from roX RNA genes into flanking chromatin. Cell. 1999 Aug 20;98(4):513–522. [PubMed]
  • Kernan MJ, Kuroda MI, Kreber R, Baker BS, Ganetzky B. napts, a mutation affecting sodium channel activity in Drosophila, is an allele of mle, a regulator of X chromosome transcription. Cell. 1991 Sep 6;66(5):949–959. [PubMed]
  • Chuang PT, Albertson DG, Meyer BJ. DPY-27:a chromosome condensation protein homolog that regulates C. elegans dosage compensation through association with the X chromosome. Cell. 1994 Nov 4;79(3):459–474. [PubMed]
  • Koonin EV, Zhou S, Lucchesi JC. The chromo superfamily: new members, duplication of the chromo domain and possible role in delivering transcription regulators to chromatin. Nucleic Acids Res. 1995 Nov 11;23(21):4229–4233. [PMC free article] [PubMed]
  • Chen JH, Lin RJ. The yeast PRP2 protein, a putative RNA-dependent ATPase, shares extensive sequence homology with two other pre-mRNA splicing factors. Nucleic Acids Res. 1990 Nov 11;18(21):6447–6447. [PMC free article] [PubMed]
  • Kuroda MI, Kernan MJ, Kreber R, Ganetzky B, Baker BS. The maleless protein associates with the X chromosome to regulate dosage compensation in Drosophila. Cell. 1991 Sep 6;66(5):935–947. [PubMed]
  • Cline TW, Meyer BJ. Vive la différence: males vs females in flies vs worms. Annu Rev Genet. 1996;30:637–702. [PubMed]
  • Company M, Arenas J, Abelson J. Requirement of the RNA helicase-like protein PRP22 for release of messenger RNA from spliceosomes. Nature. 1991 Feb 7;349(6309):487–493. [PubMed]
  • Lee CG, Hurwitz J. Human RNA helicase A is homologous to the maleless protein of Drosophila. J Biol Chem. 1993 Aug 5;268(22):16822–16830. [PubMed]
  • da Cunha PR, Granadino B, Perondini AL, Sánchez L. Dosage compensation in sciarids is achieved by hypertranscription of the single X chromosome in males. Genetics. 1994 Nov;138(3):787–790. [PMC free article] [PubMed]
  • Lee CG, Chang KA, Kuroda MI, Hurwitz J. The NTPase/helicase activities of Drosophila maleless, an essential factor in dosage compensation. EMBO J. 1997 May 15;16(10):2671–2681. [PMC free article] [PubMed]
  • de Saint Phalle B, Sullivan W. Incomplete sister chromatid separation is the mechanism of programmed chromosome elimination during early Sciara coprophila embryogenesis. Development. 1996 Dec;122(12):3775–3784. [PubMed]
  • Lee CG, da Costa Soares V, Newberger C, Manova K, Lacy E, Hurwitz J. RNA helicase A is essential for normal gastrulation. Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13709–13713. [PMC free article] [PubMed]
  • Eisen A, Lucchesi JC. Unraveling the role of helicases in transcription. Bioessays. 1998 Aug;20(8):634–641. [PubMed]
  • Lieb JD, Capowski EE, Meneely P, Meyer BJ. DPY-26, a link between dosage compensation and meiotic chromosome segregation in the nematode. Science. 1996 Dec 6;274(5293):1732–1736. [PubMed]
  • Franke A, Baker BS. The rox1 and rox2 RNAs are essential components of the compensasome, which mediates dosage compensation in Drosophila. Mol Cell. 1999 Jul;4(1):117–122. [PubMed]
  • Lieb JD, Albrecht MR, Chuang PT, Meyer BJ. MIX-1: an essential component of the C. elegans mitotic machinery executes X chromosome dosage compensation. Cell. 1998 Jan 23;92(2):265–277. [PubMed]
  • Franke A, Dernburg A, Bashaw GJ, Baker BS. Evidence that MSL-mediated dosage compensation in Drosophila begins at blastoderm. Development. 1996 Sep;122(9):2751–2760. [PubMed]
  • Lucchesi JC. Dosage compensation in Drosophila and the "complex' world of transcriptional regulation. Bioessays. 1996 Jul;18(7):541–547. [PubMed]
  • Gibson TJ, Thompson JD. Detection of dsRNA-binding domains in RNA helicase A and Drosophila maleless: implications for monomeric RNA helicases. Nucleic Acids Res. 1994 Jul 11;22(13):2552–2556. [PMC free article] [PubMed]
  • Goday C, Panzera Y, Esteban MR. A simple cytological technique to analyze nuclear divisions during preblastodermic development in Drosophila. Chromosome Res. 1999;7(6):445–448. [PubMed]
  • Marín I, Franke A, Bashaw GJ, Baker BS. The dosage compensation system of Drosophila is co-opted by newly evolved X chromosomes. Nature. 1996 Sep 12;383(6596):160–163. [PubMed]
  • Gorman M, Kuroda MI, Baker BS. Regulation of the sex-specific binding of the maleless dosage compensation protein to the male X chromosome in Drosophila. Cell. 1993 Jan 15;72(1):39–49. [PubMed]
  • McDowell KA, Hilfiker A, Lucchesi JC. Dosage compensation in Drosophila: the X chromosome binding of MSL-1 and MSL-2 in female embryos is prevented by the early expression of the Sxl gene. Mech Dev. 1996 Jun;57(1):113–119. [PubMed]
  • Gorman M, Franke A, Baker BS. Molecular characterization of the male-specific lethal-3 gene and investigations of the regulation of dosage compensation in Drosophila. Development. 1995 Feb;121(2):463–475. [PubMed]
  • Meller VH, Wu KH, Roman G, Kuroda MI, Davis RL. roX1 RNA paints the X chromosome of male Drosophila and is regulated by the dosage compensation system. Cell. 1997 Feb 21;88(4):445–457. [PubMed]
  • Meller VH, Gordadze PR, Park Y, Chu X, Stuckenholz C, Kelley RL, Kuroda MI. Ordered assembly of roX RNAs into MSL complexes on the dosage-compensated X chromosome in Drosophila. Curr Biol. 2000 Feb 10;10(3):136–143. [PubMed]
  • Hilfiker A, Hilfiker-Kleiner D, Pannuti A, Lucchesi JC. mof, a putative acetyl transferase gene related to the Tip60 and MOZ human genes and to the SAS genes of yeast, is required for dosage compensation in Drosophila. EMBO J. 1997 Apr 15;16(8):2054–2060. [PMC free article] [PubMed]
  • Meneely PM, Wood WB. Genetic analysis of X-chromosome dosage compensation in Caenorhabditis elegans. Genetics. 1987 Sep;117(1):25–41. [PMC free article] [PubMed]
  • Meyer BJ, Casson LP. Caenorhabditis elegans compensates for the difference in X chromosome dosage between the sexes by regulating transcript levels. Cell. 1986 Dec 26;47(6):871–881. [PubMed]
  • Hsu DR, Chuang PT, Meyer BJ. DPY-30, a nuclear protein essential early in embryogenesis for Caenorhabditis elegans dosage compensation. Development. 1995 Oct;121(10):3323–3334. [PubMed]
  • Palmer MJ, Mergner VA, Richman R, Manning JE, Kuroda MI, Lucchesi JC. The male-specific lethal-one (msl-1) gene of Drosophila melanogaster encodes a novel protein that associates with the X chromosome in males. Genetics. 1993 Jun;134(2):545–557. [PMC free article] [PubMed]
  • Johnston CM, Nesterova TB, Formstone EJ, Newall AE, Duthie SM, Sheardown SA, Brockdorff N. Developmentally regulated Xist promoter switch mediates initiation of X inactivation. Cell. 1998 Sep 18;94(6):809–817. [PubMed]
  • Palmer MJ, Richman R, Richter L, Kuroda MI. Sex-specific regulation of the male-specific lethal-1 dosage compensation gene in Drosophila. Genes Dev. 1994 Mar 15;8(6):698–706. [PubMed]
  • Kay GF, Penny GD, Patel D, Ashworth A, Brockdorff N, Rastan S. Expression of Xist during mouse development suggests a role in the initiation of X chromosome inactivation. Cell. 1993 Jan 29;72(2):171–182. [PubMed]
  • Pearson WR, Lipman DJ. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. [PMC free article] [PubMed]
  • Steinemann M, Steinemann S, Turner BM. Evolution of dosage compensation. Chromosome Res. 1996 Apr;4(3):185–190. [PubMed]
  • Plenefisch JD, DeLong L, Meyer BJ. Genes that implement the hermaphrodite mode of dosage compensation in Caenorhabditis elegans. Genetics. 1989 Jan;121(1):57–76. [PMC free article] [PubMed]
  • Tanaka A, Fukunaga A, Oishi K. Studies on the sex-specific lethals of Drosophila melanogaster. II. Further studies on a male-specific lethal gene, maleless. Genetics. 1976 Oct;84(2):257–266. [PMC free article] [PubMed]
  • Rastelli L, Kuroda MI. An analysis of maleless and histone H4 acetylation in Drosophila melanogaster spermatogenesis. Mech Dev. 1998 Feb;71(1-2):107–117. [PubMed]
  • Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. [PMC free article] [PubMed]
  • Rastelli L, Richman R, Kuroda MI. The dosage compensation regulators MLE, MSL-1 and MSL-2 are interdependent since early embryogenesis in Drosophila. Mech Dev. 1995 Oct;53(2):223–233. [PubMed]
  • Turner BM, Birley AJ, Lavender J. Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei. Cell. 1992 Apr 17;69(2):375–384. [PubMed]
  • Warn RM, Warn A. Microtubule arrays present during the syncytial and cellular blastoderm stages of the early Drosophila embryo. Exp Cell Res. 1986 Mar;163(1):201–210. [PubMed]
  • Richter L, Bone JR, Kuroda MI. RNA-dependent association of the Drosophila maleless protein with the male X chromosome. Genes Cells. 1996 Mar;1(3):325–336. [PubMed]
  • Wood WB, Streit A, Li W. Dosage compensation: X-repress yourself. Curr Biol. 1997 Apr 1;7(4):R227–R230. [PubMed]
  • Zhang S, Maacke H, Grosse F. Molecular cloning of the gene encoding nuclear DNA helicase II. A bovine homologue of human RNA helicase A and Drosophila Mle protein. J Biol Chem. 1995 Jul 7;270(27):16422–16427. [PubMed]
  • Scott MJ, Pan LL, Cleland SB, Knox AL, Heinrich J. MSL1 plays a central role in assembly of the MSL complex, essential for dosage compensation in Drosophila. EMBO J. 2000 Jan 4;19(1):144–155. [PMC free article] [PubMed]
  • Zhou S, Yang Y, Scott MJ, Pannuti A, Fehr KC, Eisen A, Koonin EV, Fouts DL, Wrightsman R, Manning JE, et al. Male-specific lethal 2, a dosage compensation gene of Drosophila, undergoes sex-specific regulation and encodes a protein with a RING finger and a metallothionein-like cysteine cluster. EMBO J. 1995 Jun 15;14(12):2884–2895. [PMC free article] [PubMed]
  • Smith ER, Pannuti A, Gu W, Steurnagel A, Cook RG, Allis CD, Lucchesi JC. The drosophila MSL complex acetylates histone H4 at lysine 16, a chromatin modification linked to dosage compensation. Mol Cell Biol. 2000 Jan;20(1):312–318. [PMC free article] [PubMed]

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