Skip to main content
Log in

Dosage compensation and its roles in evolution of sex chromosomes and phenotypic dimorphism: lessons from Drosophila, C.elegans and mammals

  • Review Article
  • Published:
The Nucleus Aims and scope Submit manuscript

Abstract

In many sexually reproducing species, sex is determined by cytologically distinguishable ‘sex chromosomes’. The popular view is that the consequence of heteromorphic sex chromosomes is detrimental, and evolutionary emergence of dosage compensation mechanism is expected for two fold upregulation of X linked genes in order to restore the balance for the haplo-X in the sex against the diplo X of the other. Since, male and female share nearly identical genome in most animals, and since antagonistic selection operate for the expression divergence of the sex biased genes between sexes for mating type distinction, dosage compensation system is evolved in many species to link global transcription profile of the genome through histone variants and epigenetic modification of the genes for driving sex determination function. Whole genome transcriptome analyses and the investigations on the profiling of accessible chromatin components in male and female at different phase of development of Drosophila, C. elegans and mammal revealed that 50–60% X and autosomal genes of the genomes are expressed under sex specific selection through allelic bias (except some required dosage sensitive genes) expression, ranging from absent to complete compensation. The review focuses the recent development of dosage compensation research and illustrates its roles in sex chromosome evolution and sexual dimorphism in Drosophila, C. elegans and mammals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Al Nadaf S, Waters PD, Konia E, Deakin JE, et al. Activity map of the tammar X chromosome shows that marsupial X inactivation is incomplete and escape is stochastic. Genome Biol. 2010;11:R122.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Alekseyenko AA, Demakova OV, Belyaeva ES, Makarevich GF, et al. Dosage compensation and intercalary heterochromatin in X chromosomes in Drosophila melanogaster. Chromosoma. 2002;111:106–13.

    Article  CAS  PubMed  Google Scholar 

  3. Alekseyenko AA, Ho JWK, Peng S, Gelbart M, Tolstorukov MY, et al. Sequence-specific targeting of dosage compensation in Drosophila favors an active chromatin context. PLoS Genet. 2012;8:e1002646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Arico JK, Katz DJ, Van der Vlag J, Kelly WG. Epigenetic patterns maintained in early Caenorhabditis elegans embryos can be established by gene activity in the parental germ cells. PLoS Genet. 2011;7(6):e1001391.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Assis R, Zhou Q, Bachtrog D. Sex-biased transcriptome evolution in Drosophila. Genome Biol Evol. 2012;4:1189–200.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Bachtrog D. Sex chromosome evolution: molecular aspects of Y degeneration in Drosophila. Genome Res. 2005;15:1393–401.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bachtrog D. Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet. 2013;14:113–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Bachtrog D, Charlesworth B. Reduced adaptation of a non-recombining neo-Y chromosome. Nature. 2002;416:323–6.

    Article  CAS  PubMed  Google Scholar 

  9. Bachtrog D, Hom E, Wong KM, Maside X, de Jong P. Genomic degradation of a young Y chromosome in Drosophila miranda. Genome Biol. 2008;9:R30.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Bachtrog D, Toda NRT, Lockton S. Dosage compensation and demasculinization of X chromosome in Drosophila. Curr Biol. 2010;20:1476–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bachtrog D, Kirkpatrick M, Mank JE, McDaniel SF, et al. Are all sex chromosomes created equal? Trends Genet. 2011;27(9):350–7.

    Article  CAS  PubMed  Google Scholar 

  12. Baker BS, Gorman M, Marin I. Dosage compensation in Drosophila. Annu Rev Genet. 1994;28:491–521.

    Article  CAS  PubMed  Google Scholar 

  13. Bardoni B, Zanaria E, Guioli S, Floridia G, et al. A dosage sensitive locus at chromosome Xp21 is involved in male-to-female sex reversal. Nat Genet. 1994;7:497–501.

    Article  CAS  PubMed  Google Scholar 

  14. Barr ML, Bertram EG. A morphological distinction between neurones of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Nature. 1949;163:675–7.

    Article  Google Scholar 

  15. Belote JM, Lucchesi JC. Control of X chromosome transcription by the maleless gene in Drosophila. Nature. 1980;285:573–5.

    Article  CAS  PubMed  Google Scholar 

  16. Blackman H, Ross L, Bachtrog D. Sex determination, sex chromosomes and karyotype evolution in insects. J Hered. 2016;108:1–6. https://doi.org/10.1093/jhered/esw047.

    Google Scholar 

  17. Bridges CB. Sex in relation to chromosomes. Am Nat. 1925;59:127–37.

    Article  Google Scholar 

  18. Brockdorff N, Turner BM. Dosage compensation in mammals. Cold Spring Harb Perspect Biol. 2015;7:a019406.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Brown EJ, Bachtrog D. The chromatin landscape of Drosophila: comparisons between species, sexes and chromosomes. Genome Res. 2014;24:1125–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Carvalho AB. Origin and evolution of the Drosophila Y chromosome. Cuur Opin Genet Dev. 2002;12:664–8.

    Article  CAS  Google Scholar 

  21. Carvalho AB, Koerich LB, Clark AG. Origin and evolution of Y chromosomes: Drosophila tales. Trends Genet. 2009;25:270–7.

    Article  PubMed Central  CAS  Google Scholar 

  22. Charlesworth B. Model for evolution of Y chromosome and dosage compensation. Proc Natl Acad Sci USA. 1978;75:5618–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Charlesworth B. The evolution of sex chromosomes. Science. 1991;251:1030–3.

    Article  CAS  PubMed  Google Scholar 

  24. Charlesworth B. The evolution of chromosomal sex determination and dosage compensation. Curr Biol. 1996;6:149–62.

    Article  CAS  PubMed  Google Scholar 

  25. Charlesworth D, Charlesworth B, Marais G. Steps in the evolution of heteromorphic sex chromosomes. Heredity. 2005;95:118–28.

    Article  CAS  PubMed  Google Scholar 

  26. Chattejree SN, Mukherjee AS. Chromosomal basis of dosage compensation in Drosophila.V. Puffwise analysis of gene activity in the X-chromosome of male and female of D. hydei. Chromosoma. 1971;36:46–59.

    Article  Google Scholar 

  27. Chatterjee RN. X chromosomal organization and dosage compensation: in situ transcription of chromatin template activity of X chromosome hyperploids of Drosophila melanogaster. Chromosoma. 1985;91:259–66.

    Article  CAS  PubMed  Google Scholar 

  28. Chatterjee RN. Mosaic pattern of X chromosomal transcriptions in a strain of Drosophila melanogaster with aneuploid X chromosome. Ind J Exp Biol. 1990;28:101–5.

    CAS  Google Scholar 

  29. Chatterjee RN. Binding affinity of leucine containing chromatin proteins to the polytene X chromosome of Drosophila and its significance. Ind J Exp Biol. 1991;29:301–4.

    CAS  Google Scholar 

  30. Chatterjee RN. Mechanisms of X chromosome regulation in Drosophila melanogaster. Nucleus. 1992;35:31–44.

    Google Scholar 

  31. Chatterjee RN. Mechanisms and evolutionary origins of gene dosage compensation. In: Chatterjee RN, Sanchez L, editors. Genome analysis in eukaryotes: developmental and evolutionary aspects. Narosa: Springer; 1998. p. 167–214.

    Chapter  Google Scholar 

  32. Chatterjee RN, Chatterjee P. Evolutionary origin of chromatin remodeling for dosage compensation: lessons from epigenetic modifications of X chromosomes in germ cells of Drosophila C. elegans and mammals. Nucleus. 2012;55:3–16.

    Article  Google Scholar 

  33. Chatterjee RN, Mukherjee AS. Chromosomal basis of dosage compensation in Drosophila. IX. Cellular autonomy of the faster replication of X chromosome in haplo X cells of Drosophila melanogaster and synchronous initiation. J Cell Biol. 1977;74:168–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Chatterjee RN, Mukherjee AS. Chromosomal basis of dosage compensation in Drosophila: assessment of hyperactivity of male X in situ. J Cell Sci. 1981;47:295–309.

    CAS  PubMed  Google Scholar 

  35. Chatterjee RN. The evolution of sex determination pathway: reasoning from Drosophila. Presidential Lecture of Animal Science Section. Indian Science Congress Association. 2003; pp. 1–40.

  36. Chatterjee RN, Derksen J, Van Der Ploeg M, Mukherjee AS. Role of nonhistone chromosomal protein in attainment of hyperactivity of the X chromosome of male Drosophila: a quantitative cytochemical study. Ind J Exp Biol. 1980;18:574–5.

    CAS  Google Scholar 

  37. Chatterjee RN, Dube DK, Mukherjee AS. In situ transcription analysis of chromatin template activity of the X chromosome of Drosophila following high molar NaCl treatment. Chromosoma. 1981;82:515–23.

    Article  CAS  PubMed  Google Scholar 

  38. Chatterjee RN, Chatterjee R, Ghosh S. Heterochromatin-binding proteins regulate male X polytene chromosome morphology and dosage compensation: an evidence from a variegated rearranged strain [In (1)BM 2,(rv)] and its interactions with hyperploids and mle mutation in Drosophila melanogaster. Nucleus. 2016;59:141–54.

    Article  Google Scholar 

  39. Chaumeil J, Waters PD, Koina E, Gilbert C, Robinson TJ, et al. Evolution from XIST-independent to XIST-controlled X chromosome inactivation: epigenetic modifications in distantly related mammals. PLoS One. 2011;6(4):e19040.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Chen Zhang J. No X chromosome dosage compensation in human proteomes. Mol Biol Evol. 2015;32:1456–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Cline TW, Meyer BJ. Vive La difference: males vs females in flies vs worms. Annu Rev Genet. 1996;30:637–702.

    Article  CAS  PubMed  Google Scholar 

  42. Conrad T, Akhtar A. Dosage compensation in Drosophila melanogaster: epigenetic fine-tuning of chromosome-wide transcription. Nature Rev Genet. 2012;13:123–34.

    Article  CAS  PubMed  Google Scholar 

  43. Csankovszki G, Collette K, Spahl K, Carey J, Snyder M, Petty E, Patel U, TabuchiT Liu H, McLeod I, et al. Three distinct condensin complexes control C. elegans chromosome dynamics. Curr Biol. 2009;19:9–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Das M, Mutsuddi D, Duttagupta AK, Mukherjee AS. Segmental heterogenety in replication and transcription of X2 chromosome in Drosophila miranda and conservativeness in the evolution of dosage compensation. Chromosoma. 1982;87:373–88.

    Article  CAS  Google Scholar 

  45. Dawes HE, Berlin DS, Lapidus DM, Nusbaum C, Davis TL, Meyer BJ. Dosage compensation proteins targeted to X chromosomes by a determinant of hermaphrodite fate. Science. 1999;284:1800–4.

    Article  CAS  PubMed  Google Scholar 

  46. Demakova OV, Kotlikova IV, Gordadze PR, Alekseyenko AA, et al. The MSL complex levels are critical for its correct targeting to the chromosomes in Drosophila melanogaster. Chromosoma. 2003;112:103–15.

    Article  CAS  PubMed  Google Scholar 

  47. Deng X, Koya SK, Kong Y, Meller VH. Coordinated regulation of heterochromatic genes in Drosophila melanogaster. Genetics. 2009;182:481–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Deng X, Berletch JB, Ma W, et al. Mammalian X upregulation is associated with enhanced transcription initiation, RNA half-life, and MOF-mediated H4K16 acetylation. Dev Cell. 2013;25:55–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Deuring R, Fanti L, Armstrong JA, Sarte M, Papoulas O, et al. The ISWI chromatin-remodeling protein is required for gene expression and the maintenance of higher order chromatin structure in vivo. Mol Cell. 2000;5:355–65.

    Article  CAS  PubMed  Google Scholar 

  50. DiBartolomeis SM, Tartof KD, Jackson FR. A superfamily of Drosophila satellite related (SR) DNA repeats restricted to the X chromosome euchromatin. Nucleic Acids Res. 1992;20:1113–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Dimitri P, Junakovic N, Arcà B. Colonization of heterochromatic genes by transposable elements in Drosophila. Mol Biol Evol. 2003;20:503–12.

    Article  CAS  PubMed  Google Scholar 

  52. Disteche CM. Dosage Compensation of the Sex Chromosomes. Annu Rev Genet. 2012;46:537–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Ellegren H. Sex-chromosome evolution: recent progress and the influence of male and female heterogamety. Nature Rev Genet. 2011;12:157–66.

    Article  CAS  PubMed  Google Scholar 

  54. Ellegren H, Parsch J. The evolution of sex biased genes and sex—biased gene expression. Nat Rev Genet. 2007;8:689–98.

    Article  CAS  PubMed  Google Scholar 

  55. Ellison C, Bachtrog D. Non-allelic gene conversion enables rapid evolutionary changes at multiple regulatory sites encoded by transposable elements. eLIFE. 2015;4:e05899. doi:10.7554/eLife.05899.

    Article  PubMed Central  CAS  Google Scholar 

  56. Fagegaltier D, König A, Lai A, Gordon EC, Gingeras TR, et al. A genome-wide survey of sexually dimorphic expression of Drosophila miRNAs identifies the steroid hormone-induced miRNA let-7 as a regulator of sexual identity. Genetics. 2014;198:647–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Gallach M, Betrán E. Dosage compensation and the distribution of sex-biased gene expression in Drosophila: considerations and genomic constraints. J Mol Evol. 2016;82:199–206.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Gelbart ME, Kuroda M. Drosophila dosage compensation: a complex voyage to the X chromosome. Development. 2009;136:1399–410.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Gibson JR, Chippindale AK, Rice WR. The X chromosome is a hot spot for sexually antagonistic fitness variation. Proc Roy Soc Lond B. 2002;269:499–505.

    Article  Google Scholar 

  60. Gladstein N, McKeon MN, Horabin JI. Requirement of male-specific dosage compensation in Drosophila females—implications of early X chromosome gene expression. PLoS Genet. 2010;6(7):e100104.

    Article  CAS  Google Scholar 

  61. Graves JAM. Avian sex, sex chromosomes, and dosage compensation in the age of genomics. Chromosome Res. 2014;22:45–57.

    Article  PubMed  CAS  Google Scholar 

  62. Graves JAM. Evolution of vertebrate sex chromosomes and dosage compensation. Nature Rev Genet. 2016;17:33–46.

    Article  CAS  PubMed  Google Scholar 

  63. Gu T, Elgin SC. Maternal depletion of Piwi, a component of the RNAi system, impacts heterochromatin formation in Drosophila. PLoS Genet. 2013;9:e1003780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Gupta V, Parisi M, Sturgill D, Nuttall R, Doctolero M, et al. Global analysis of X-chromosome dosage compensation. J Biol. 2006;5:3.1–3.10.

    Article  CAS  Google Scholar 

  65. Hamada FN, Park PJ, Gordadze PR, Kuroda MI. Global regulation of X chromosomal genes by the MSL complex in Drosophila melanogaster. Genes Dev. 2005;19:2289–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Hense W, Baines JF, Parsch J. X chromosome inactivation during Drosophila spermatogenesis. PLoS Biol. 2007;5:e273.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Hodgkin J. Primary sex determination in the nematode C. elegans. Development. 1987;101(Suppl):5–15.

    PubMed  Google Scholar 

  68. Huijser P, Hennig W, Dijkhof R. Poly (dC-dA/dG-dT) repeats in the Drosophila genome: a key function for dosage compensation and position effect? Chromosoma. 1987;95:209–15.

    Article  CAS  Google Scholar 

  69. Huylmans AK, Parsch J. Variation in the X: autosome distribution of male-biased genes among Drosophila melanogaster tissues and its relationship with dosage compensation. Genome Biol Evol. 2015;7:1960–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Huynh KD, Lee JT. Inheritance of a pre-inactivated paternal X chromosome in early mouse embryos. Nature. 2003;426:857–62.

    Article  CAS  PubMed  Google Scholar 

  71. Joshi SS, Meller VH. Satellite repeats identify X chromatin for dosage compensation in Drosophila melanogaster males. Curr Biol. 2017;27:1–10.

    Article  CAS  Google Scholar 

  72. Khil PP, Smirnova NA, Romanienko PJ, Camerini-Otero RD. The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat Genet. 2004;36:642–6.

    Article  CAS  PubMed  Google Scholar 

  73. Kotlikova IV, Demakova OV, Semeshin VF, Shloma VV, Boldyreva LV, Kuroda MI, Zhimulev IF. The Drosophila dosage compensation complex binds to polytene chromosomes independently of developmental changes in transcription. Genetics. 2006;172:963–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Koya SK, Meller VH. Modulation of heterochromatin by male specific lethal proteins and roX RNA in Drosophila melanogaster males. PLoS One. 2015;10(10):e0140259.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Kuroda MI, Hilfiker A, Lucchesi JC. Dosage compensation in Drosophila—a model for coordinate regulation of transcription. Genetics. 2016;204:435–50.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Lakhotia SC, Mukherjee AS. Chromosomal basis of dosage compensation in Drosophila. I. Cellular autonomy of hyperactivity of male X-chromosome in salivary glands and sex differentiation. Genet Res. 1969;14:137–50.

    Article  CAS  PubMed  Google Scholar 

  77. Lakhotia SC, Mukherjee AS. Chromosomal basis of dosage compensation in Drosophila. III. Early completion of replication by polytene the polytene X chromosome in male: further evidence and its implications. J Cell Biol. 1970;47:18–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Lakhotia SC, Mukherjee AS. Chromosomal basis of dosage compensation in Drosophila. IV, Hyperactivity of X-chromosome in male of D. bipectinata and D. kikkawai. Proc Zool Soc (Calcutta). 1972;25:1–9.

    Google Scholar 

  79. Lifschytz E, Lindsley DL. The role of X-chromosome inactivation during spermatogenesis. Proc Natl Acad Sci USA. 1972;69:182–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Lin MF, Carlson JW, Crosby MA, Matthews BB, et al. Revisiting the protein—coding gene catalog of Drosophila melanogaster using 12 fly genomes. Geneome Res. 2007;17:1823–36.

    Article  CAS  Google Scholar 

  81. Livernosis AM, Graves JAM, Waters PD. The origin and evolution of vertebrate sex chromosomes and dosage compensation. Heredity. 2012;108:50–8.

    Article  Google Scholar 

  82. Lott SE, Villalta JE, Schroth GP, Luo S, Tonkin LA, et al. Noncanonical compensation of zygotic X transcription in early Drosophila melanogaster development revealed through single-embryo RNA-Seq. PLoS Biol. 2011;9:e1000590.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Lucchesi JC. Gene dosage compensation and the evolution of sex chromosomes. Science. 1978;202:711–6.

    Article  CAS  PubMed  Google Scholar 

  84. Lucchesi JC, Manning JE. Gene dosage compensation in Drosophila melanogaster. Adv Genet. 1987;24:371–429.

    CAS  PubMed  Google Scholar 

  85. Lucchesi JC, Rawls RM Jr. Regulation of gene function: a comparison of X linked enzyme activity levels in normal and intersexual triploids of Drosophila melanogaster. Genetics. 1973;73:459–64.

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Lucchesi JC, Rawls JM Jr, Maroni G. Gene dosage compensation in metafemales (3X; 2A) of Drosophila. Nature. 1974;248:564–7.

    Article  CAS  PubMed  Google Scholar 

  87. Lucchesi JC, Belote JM, Maroni G. X-linked gene activity in metamales (XY; 3A) of Drosophila. Chromosoma. 1977;65:1–7.

    Article  CAS  Google Scholar 

  88. Lucchesi JC, Kelly WG, Panning B. Chromatin remodeling in dosage compensation. Annu Rev Genet. 2005;39:615–51.

    Article  CAS  PubMed  Google Scholar 

  89. Lyon MF. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature. 1961;190:372–3.

    Article  CAS  PubMed  Google Scholar 

  90. Lyon MF. X-chromosome inactivation. Curr Biol. 1998;9:R235–7.

    Article  Google Scholar 

  91. Maclaughlin DT, Donahoe PK. Mechanisms of disease sex determination and differentiation. N Engl J Med. 2004;350:4.

    Article  Google Scholar 

  92. Mank JE. The transcriptional architecture of phenotypic dimorphism. Nat Ecol Evol. 2017; 1.0006. https://doi.org/10.1038/s41559.016/0006.

  93. Mank JE, Hosken DJ, Wedell N. Some inconvenient truths about sex chromosome dosage compensation and the potential role of sexual conflict. Evolution. 2011;65:2133–44.

    Article  PubMed  Google Scholar 

  94. Maroni G, Lucchesi JC. X chromosome transcription in Drosophila. Chromosoma. 1980;77:253–61.

    Article  CAS  PubMed  Google Scholar 

  95. Maroni G, Plaut W. Dosage compensation in Drosophila melanogaster triploids. I. Autoradiographic study. Chromosoma. 1973;40:361–77.

    Article  CAS  PubMed  Google Scholar 

  96. McQueen HA, McBride D, Miele G, Bird AP, et al. Dosage compensation in birds. Cell Curr Biol. 2001;11:253–7.

    CAS  PubMed  Google Scholar 

  97. Meller VH, Rattner BP. The roX genes encode redundant male specific lethal transcripts required for targeting of the MSL complex. EMBO J. 2002;21:1084–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Menon DU, Meller VH. Imprinting of the Y chromosome influences dosage compensation in roX1 and roX2 Drosophila melanogtaster. Genetics. 2009;183:811–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Meyer BJ. Sex in the worm counting and compensating X-chromosome dose. Trends Genet. 2000;16:247–53.

    Article  CAS  PubMed  Google Scholar 

  100. Moore KL, Barr ML. Morphology of the nerve cell nucleus in mammals, with special reference to the sex chromatin. J Comp Neurol. 1953;98:213–31.

    Article  CAS  PubMed  Google Scholar 

  101. Mukherjee AS, Beermann W. Synthesis of ribonucleic acid by the X-chromosomes of Drosophila melanogaster and the problem of dosage compensation. Nature. 1965;207:785–6.

    Article  CAS  PubMed  Google Scholar 

  102. Mukherjee J, Chatterjee RN. In situ transcription analysis of chromatin template activity of the X chromosome in meta males (XY; 3A) and intersexes (2X; 3A) of Drosophila melanogaster. Proc Zool Soc. 1992;45(Suppl A):265–75.

    Google Scholar 

  103. Muller HJ. Evidence of the precision of genetic adaptation. Harvey Lect Ser. 1950;43:165–229.

    Google Scholar 

  104. Muller HJ. Further studies on the nature and causes of gene mutations. In: Proceedings of the Sixth International Congress of Genetics, Ithaca, NY; 1932; 1: 213–55.

  105. Nguyen DK, Disteche CM. Dosage compensation of the active X chromosome in mammals. Nat Genet. 2006;38:47–53.

    Article  CAS  PubMed  Google Scholar 

  106. Nicoll M, Akerib CC, Meyer BJ. X-chromosome-counting mechanisms that determine nematode sex. Nature. 1997;388:200–4.

    Article  CAS  PubMed  Google Scholar 

  107. Ohno S. Sex chromosomes and sex-linked genes. Berlin: Springer; 1967.

    Book  Google Scholar 

  108. Ohno S, Kaplan WD, Kinosita R. Formation of the sex chromatin by a single X-chromosome in liver cells of Rattus norvegicus. Exp Cell Res. 1959;18:415–8.

    Article  CAS  PubMed  Google Scholar 

  109. Oliver B, Parisi M. Battle of the Xs. BioEssays. 2004;26:543–8.

    Article  PubMed  Google Scholar 

  110. Palmer MJ, Mergner VA, Richman R, Manning JE, Kuroda MI, et al. 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;134:545–57.

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Parisi M, Nuttall R, Naiman D, Bouffard G, Malley J, et al. Paucity of genes on the Drosophila X chromosome showing male biased expression. Science. 2003;299:697–700.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Payer B, Lee JT. X chromosome dosage compensation: how mammals keep the balance. Annu Rev Genet. 2008;42:733–72.

    Article  CAS  PubMed  Google Scholar 

  113. Petty EL, Collette KS, Cohen AJ, Snyder MJ, Csankovszki G. Restricting dosage compensation complex binding to the X chromosomes by H2A.Z/HTZ-1. PLoS Genet. 2009;5:e1000699.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  114. Philip P, Stenberg P. Male X linked genes in Drosophila melanogaster are compensated independently of male specific lethal complex. Epigenet Chromatin. 2013;6:35.

    Article  Google Scholar 

  115. Pimpinelli S, Berloco M, Fanti L, Dimitri P, Bonaccorsi S, Marchetti E, Caizzi R, Caggese C, Gatti M. Transposable elements are stable structural components of Drosophila melanogaster heterochromatin. Proc Natl Acad Sci USA. 1995;92:3804–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Pindyurin AV, Boldyreva LV, Shiome VV, Kolesnikova TD, et al. Interaction between the Drosophila heterochromatin proteins SUUR and HP1. J Cell Sci. 2008;121:1693–703.

    Article  CAS  PubMed  Google Scholar 

  117. Ranz JM, Castillo-Davis CI, Meiklejohn CD, Hartl DL. Sex dependent gene expression and evolution of the Drosophila transcriptome. Science. 2003;300:1742–5.

    Article  CAS  PubMed  Google Scholar 

  118. Rice W. Sex chromosomes and the evolution of sexual dimorphism. Evolution. 1984;2002:735–42.

    Article  Google Scholar 

  119. Rice WR. Sexually antagonistic genes-experimental evidence. Science. 1992;256:1436–9.

    Article  CAS  PubMed  Google Scholar 

  120. Sala A, Toto M, Pinello L, et al. Genome-wide characterization of chromatin binding and nucleosome spacing activity of the nucleosome remodelling ATPase ISWI. EMBO J. 2011;30:1766–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Skripsky T, Lucchesi JC. Intersexuality resulting from interaction of sex specific lethal mutations in Drosophila melanogaster. Dev Biol. 1982;94:153–62.

    Article  CAS  PubMed  Google Scholar 

  122. Smith PD, Lucchesi JC. The role of sexuality in dosage compensation in Drosophila. Genetics. 1968;61:607–18.

    Google Scholar 

  123. Spierer A, Seum C, Delattre M, Spierer P. Loss of the modifiers of variegation Su(var)3-7 or HP1 impacts male X polytene chromosome morphology and dosage compensation. J Cell Sci. 2005;118:5047–57.

    Article  CAS  PubMed  Google Scholar 

  124. Steinemann M, Steinemann S, Lottspeich F. How Y chromosomes become genetically inert? Proc Natl Acad Sci USA. 1993;90:5737–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Steinmann-Zwicky M, Nothiger R. A small region on the X chromosome of Drosophila regulates a key gene that controls sex determination and dosage compensation. Cell. 1985;42:877–87.

    Article  CAS  PubMed  Google Scholar 

  126. Stewart BR, Merriam JR. Dosage compensation. In: Ashburner M, Wright TRF, editors. The genetics and biology of Drosophila. 2nd ed. New York: Academic Press; 1980. p. 107–40.

    Google Scholar 

  127. Strome S, Kelly WG, Ercan S, Lieb JD. Regulation of the X chromosomes in Caenorhaditis elegans. Cold Spring Harbor Perspect Biol. 2014; 6. https://doi.org/10.1101/cshperspect.a018366.

  128. Sturgill D, Zhang Y, Parisi M, Oliver B. Demasculinization of X chromosomes in the Drosophila genus. Nature. 2007;450:238–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Sulston JE, Schierenberg E, White JG, Thomson JN. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol. 1983;100:64.

    Article  CAS  PubMed  Google Scholar 

  130. Swaminathan J, Baxter EL, Corces VG. The role of histone H2Av variant replacement and histone H4 acetylation in the establishment of Drosophila heterochromatin. Genes Dev. 2005;19:65–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Taipale M, Akhtar A. Chromatin mechanisms in Drosophila dosage compensation. Prog Mol Cell Biol. 2005;38:123–49.

    CAS  Google Scholar 

  132. Turner JMA. Meiotic sex chromosome inactivation. Development. 2007;134:1823–31.

    Article  CAS  PubMed  Google Scholar 

  133. Vaqueriza JM, Torres-Padilla ME. Panoramic views of early epigenome. Nature. 2016;537:494–6.

    Article  CAS  Google Scholar 

  134. Vensko SP II, Stone EA. No evidence for a global male-specific lethal complex-mediated dosage compensation contribution to the demasculinization of the Drosophila melanogaster X chromosome. PLoS One. 2014;9:e103659.

    Article  PubMed  PubMed Central  Google Scholar 

  135. Veyrunes F, Waters PD, Miethke P, et al. Bird like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Res. 2008;18:965–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Vicoso B, Bachtrog D. Progress and prospects toward our understanding of the evolution of dosage compensation. Chromosome Res. 2009;17:585–602.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Vicoso B, Charlesworth B. The deficit of male-biased genes on the D. melanogaster X chromosome is expression-dependent: a consequence of dosage compensation? J Mol Evol. 2009;68:576–83.

    Article  CAS  PubMed  Google Scholar 

  138. Wang PJ, McCarrey JR, Yang F, Page DC. An abundance of X linked genes expressed in spermatogonia. Nat Genet. 2001;27:422–6.

    Article  PubMed  CAS  Google Scholar 

  139. Wang Q, Mank JE, Li J, Yang N, Qu L. Allele-specific expression analysis does not support sex chromosome inactivation on the chicken Z chromosome. Genome Biol Evol. 2017;9(3):619–26. https://doi.org/10.1093/gbe/evx031.

    Article  PubMed  PubMed Central  Google Scholar 

  140. Waring GL, Pollack JC. Cloning and characterization of a dispersed, multicopy, X chromosome sequence in Drosophila melanogaster. Proc Natl Acad Sci USA. 1987;84:2843–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Waters PD, Wallis MC, Graves JAM. Mammalian sex—Origin and evolution of the Y chromosome and SRY. Semin Cell Dev Biol. 2007;18:389–400.

    Article  CAS  PubMed  Google Scholar 

  142. Wright AE, Dean R, Zimmer F, Mank JE. How to make a sex chromosome? Nat Commun. 2016;7:12087.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Wu J, Huang B, Chen H, et al. The landscape of accessible chromatin in mammalian pre-implantation embryos. Nature. 2016;534:652–7.

    Article  CAS  PubMed  Google Scholar 

  144. Wutz A. Gene silencing in X-chromosome inactivation: advances in understanding facultative heterochromatin formation. Nat Rev Genet. 2011;12:542–53.

    Article  CAS  PubMed  Google Scholar 

  145. Zhang Y, Oliver B. An evolutionary consequence of dosage compensation on Drosophila melanogaster female X-chromatin structure? BMC Genom. 2010;11:6.

    Article  CAS  Google Scholar 

  146. Zhang W, Deng H, Bao X, Lerach S, Girton J, et al. The JIL-1 histone H3S10 kinase regulates dimethyl H3K9 modifications and heterochromatic spreading in Drosophila. Development. 2006;133:229–35.

    Article  CAS  PubMed  Google Scholar 

  147. Zhang Y, Sturgill D, Parisi M, Kumar S, Oliver B. Constraint and turnover in sex-biased gene expression in the genus Drosophila. Nature. 2007;450:233–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Zhimulev IF, Belyaeva ES, Semeshin VF, Shloma VV, et al. Overexpression of SuUR gene induces reversible modifications at pericentric, telomeric and intercalary heterochromatin of Drosophila melanogaster polytene chromosomes. J Cell Sci. 2003;116:169–76.

    Article  CAS  PubMed  Google Scholar 

  149. Zhou Q, Zhu H-M, Huang Q-F, Zho L, et al. Deciphering neo-sex and B chromosome evolution by the draft genome of Drosophila albomicans. BMC Genom. 2012;13:109.

    Article  CAS  Google Scholar 

  150. Zhou Q, Ellison CE, Kaiser VB, Alekseyenko AA, Gorchakov AA, et al. The epigenome of evolving Drosophila neo-sex chromosomes: dosage compensation and heterochromatin formation. PLoS Biol. 2013;11:e1001711.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

The work has been supported by UGC Emeritus Fellowship [Sanction No. F. 6-6/2015-17/EMERITUS-2015-17-GEN-5478(SA-II) dt.21.09.2015] to RNC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. N. Chatterjee.

Additional information

In Honour of Prof AK Sharma, the Founder and Editor-in-Chief of the Nucleus.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chatterjee, R.N. Dosage compensation and its roles in evolution of sex chromosomes and phenotypic dimorphism: lessons from Drosophila, C.elegans and mammals. Nucleus 60, 315–333 (2017). https://doi.org/10.1007/s13237-017-0223-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13237-017-0223-6

Keywords

Navigation