Table of Contents
Advances in Evolutionary Biology
Volume 2014 (2014), Article ID 104683, 9 pages
http://dx.doi.org/10.1155/2014/104683
Review Article

Repetitive Sequence and Sex Chromosome Evolution in Vertebrates

Institute for Applied Ecology, University of Canberra, Canberra, ACT 2601, Australia

Received 14 May 2014; Accepted 3 September 2014; Published 11 September 2014

Academic Editor: Paul Harrison

Copyright © 2014 Tariq Ezaz and Janine E. Deakin. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. Henking, “Über Patagonian pejerrey (Odontesthes hatcheri) spermatogenese und deren Beziehung zur Entwicklung bei Pyrrhocoris apterus L,” Zeitschrift für Wissenschaftliche Zoologie, vol. 51, pp. 685–736, 1891. View at Google Scholar
  2. N. M. Stevens, Studies in Spermatogenesis with Especial Reference to the “Accessory Chromosome”, vol. 36, Carnegie Institution of Washington Publication, 1905.
  3. E. B. Wilson, “The chromosomes in relation to the determination of sex in insects,” Science, vol. 22, pp. 500–502, 1905. View at Google Scholar · View at Scopus
  4. J. F. Hughes, H. Skaletsky, L. G. Brown et al., “Strict evolutionary conservation followed rapid gene loss on human and rhesus y chromosomes,” Nature, vol. 483, no. 7387, pp. 82–87, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. J. F. Hughes, H. Skaletsky, T. Pyntikova et al., “Chimpanzee and human y chromosomes are remarkably divergent in structure and gene content,” Nature, vol. 463, no. 7280, pp. 536–539, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. G. Li, B. W. Davis, T. Raudsepp et al., “Comparative analysis of mammalian y chromosomes illuminates ancestral structure and lineage-specific evolution,” Genome Research, vol. 23, no. 9, pp. 1486–1495, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Skaletsky, T. Kuroda-Kawaguchl, P. J. Minx et al., “The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes,” Nature, vol. 423, no. 6942, pp. 825–837, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Chen, G. Zhang, C. Shao et al., “Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle,” Nature Genetics, vol. 46, no. 3, pp. 253–260, 2014. View at Google Scholar
  9. C. L. Peichel, J. A. Ross, C. K. Matson et al., “The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome,” Current Biology, vol. 14, no. 16, pp. 1416–1424, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Kondo, U. Hornung, I. Nanda et al., “Genomic organization of the sex-determining and adjacent regions of the sex chromosomes of medaka,” Genome Research, vol. 16, no. 7, pp. 815–826, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. D. Charlesworth, B. Charlesworth, and G. Marais, “Steps in the evolution of heteromorphic sex chromosomes,” Heredity, vol. 95, no. 2, pp. 118–128, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. T. Ezaz, S. D. Sarre, D. O'Meally, J. A. Marshall Graves, and A. Georges, “Sex chromosome evolution in lizards: independent origins and rapid transitions,” Cytogenetic and Genome Research, vol. 127, no. 2–4, pp. 249–260, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Bernardo Carvalho and A. G. Clark, “Efficient identification of y chromosome sequences in the human and drosophila genomes,” Genome Research, vol. 23, no. 11, pp. 1894–1907, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. J. J. Bull, Evolution of Sex Determining Mechanisms, Benjamin/Cummings Publishing Company, Menlo Park, Calif, USA, 1983.
  15. S. Ohno, Sex Chromosomes and Sex-Linked Genes, Springer, Heidelberg, Germany, 1967.
  16. A. J. Solari, Sex Chromosomes and Sex Determination in Vertebrates, CRC Press, Boca Raton, Fla, USA, 1993.
  17. B. Charlesworth, “The evolution of sex chromosomes,” Science, vol. 251, no. 4997, pp. 1030–1033, 1991. View at Publisher · View at Google Scholar · View at Scopus
  18. W. R. Rice, “Evolution of the Y sex chromosome in animals,” BioScience, vol. 46, no. 5, pp. 331–343, 1996. View at Publisher · View at Google Scholar · View at Scopus
  19. J. F. Hughes, H. Skaletsky, T. Pyntikova et al., “Conservation of Y-linked genes during human evolution revealed by comparative sequencing in chimpanzee.,” Nature, vol. 437, no. 7055, pp. 100–103, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. H. K. Moghadam, M. A. Pointer, A. E. Wright, S. Berlin, and J. E. Mank, “W chromosome expression responds to female-specific selection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 21, pp. 8207–8211, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. H. J. Muller, “A gene for the fourth chromosome of Drosophila,” Journal of Experimental Zoology, vol. 17, pp. 325–336, 1914. View at Google Scholar
  22. T. Ezaz, R. Stiglec, F. Veyrunes, and J. A. Marshall Graves, “Relationships between vertebrate ZW and XY sex chromosome systems,” Current Biology, vol. 16, no. 17, pp. R736–R743, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. J. A. M. Graves, “Sex chromosome specialization and degeneration in mammals,” Cell, vol. 124, no. 5, pp. 901–914, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. J. E. Mank, “Small but mighty: the evolutionary dynamics of W and y sex chromosomes,” Chromosome Research, vol. 20, no. 1, pp. 21–33, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. I. Miura, H. Ohtani, and M. Ogata, “Independent degeneration of W and y sex chromosomes in frog Rana rugosa,” Chromosome Research, vol. 20, no. 1, pp. 47–55, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. D. O'Meally, T. Ezaz, A. Georges, S. D. Sarre, and J. A. M. Graves, “Are some chromosomes particularly good at sex? Insights from amniotes,” Chromosome Research, vol. 20, no. 1, pp. 7–19, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. S. D. Sarre, T. Ezaz, and A. Georges, “Transitions between sex-determining systems in reptiles and amphibians,” Annual Review of Genomics and Human Genetics, vol. 12, pp. 391–406, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Fisher, “The evolution of dominance,” Biological Reviews, vol. 6, no. 4, pp. 345–368, 1931. View at Google Scholar
  29. B. Charlesworth and D. Charlesworth, “The degeneration of Y chromosomes,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 355, no. 1403, pp. 1563–1572, 2000. View at Publisher · View at Google Scholar · View at Scopus
  30. J. A. M. Graves and C. L. Peichel, “Are homologies in vertebrate sex determination due to shared ancestry or to limited options?” Genome Biology, vol. 11, no. 4, article 205, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. N. Perrin, “Sex reversal: a fountain of youth for sex chromosomes?” Evolution, vol. 63, no. 12, pp. 3043–3049, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Nei, “Linkage modifications and sex difference in recombination.,” Genetics, vol. 63, no. 3, pp. 681–699, 1969. View at Google Scholar · View at Scopus
  33. J. A. M. Graves, “Review: sex chromosome evolution and the expression of sex-specific genes in the placenta,” Placenta, vol. 31, pp. S27–S32, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. D. Dumas and J. Britton-Davidian, “Chromosomal rearrangements and evolution of recombination: comparison of chiasma distribution patterns in standard and Robertsonian populations of the house mouse,” Genetics, vol. 162, no. 3, pp. 1355–1366, 2002. View at Google Scholar · View at Scopus
  35. C. O. Ostberg, L. Hauser, V. L. Pritchard, J. C. Garza, and K. A. Naish, “Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss),” BMC Genomics, vol. 14, no. 1, article 570, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. R. H. Devlin and Y. Nagahama, “Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences,” Aquaculture, vol. 208, no. 3-4, pp. 191–364, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. C. Eggert, “Sex determination: the amphibian models,” Reproduction Nutrition Development, vol. 44, no. 6, pp. 539–549, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Schartl, “Sex chromosome evolution in non-mammalian vertebrates,” Current Opinion in Genetics and Development, vol. 14, no. 6, pp. 634–641, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Schmid, I. Nanda, C. Steinlein, K. Kausch, T. Haaf, and J. T. Epplen, “Chapter 16—sex-determining mechanisms and sex chromosomes in amphibia,” in Amphibian Cytogenetics and Evolution, D. M. Green and S. K. Sessions, Eds., pp. 393–430, Academic Press, San Diego, Calif, USA, 1991. View at Publisher · View at Google Scholar
  40. O. Blaser, C. Grossen, S. Neuenschwander, and N. Perrin, “Sex-chromosome turnovers induced by deleterious mutation load,” Evolution, vol. 67, no. 3, pp. 635–645, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. M. B. Cioffi and L. A. C. Bertollo, “Chromosomal distribution and evolution of repetitive DNAs in Fish,” Genome Dynamics, vol. 7, pp. 197–221, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. K. Matsubara, T. Knopp, S. D. Sarre, A. Georges, and T. Ezaz, “Karyotypic analysis and FISH mapping of microsatellite motifs reveal highly differentiated XX/XY sex chromosomes in the pink-tailed worm-lizard (Aprasia parapulchella, Pygopodidae, Squamata),” Molecular Cytogenetics, vol. 6, no. 1, article 60, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Matsubara, S. D. Sarre, A. Georges, Y. Matsuda, J. A. Marshall Graves, and T. Ezaz, “Highly differentiated ZW sex microchromosomes in the australian varanus species evolved through rapid amplification of repetitive sequences,” PLoS ONE, vol. 9, no. 4, Article ID e95226, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. M. B. Cioffi, J. P. M. Camacho, and L. A. C. Bertollo, “Repetitive DNAs and differentiation of sex chromosomes in neotropical fishes,” Cytogenetic and Genome Research, vol. 132, no. 3, pp. 188–194, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. M. B. Cioffi, E. Kejnovsky, and L. A. C. Bertollo, “The chromosomal distribution of microsatellite repeats in the genome of the wolf fish Hoplias malabaricus, focusing on the sex chromosomes,” Cytogenetic and Genome Research, vol. 132, no. 4, pp. 289–296, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. S. G. Durkin and T. W. Glover, “Chromosome fragile sites,” Annual Review of Genetics, vol. 41, pp. 169–192, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. L. D. Hurst and H. Ellegren, “Sex biases in the mutation rate,” Trends in Genetics, vol. 14, no. 11, pp. 446–452, 1998. View at Publisher · View at Google Scholar · View at Scopus
  48. E. Olmo, “Reptilia,” in Animal Cytogenetics Volume 4: Chordata, B. John, Ed., part 3, Gebrüder Borntraeger, Berlin, Germany, 1986. View at Google Scholar
  49. K. M. Reed and R. B. Phillips, “Polymorphism of the nucleolus organizer region (NOR) on the putative sex chromosomes of Arctic char (Salvelinus alpinus) is not sex related,” Chromosome Research, vol. 5, no. 4, pp. 221–227, 1997. View at Publisher · View at Google Scholar · View at Scopus
  50. K. Matsubara, T. Gamble, Y. Matsuda et al., “Non-homologous sex chromosomes in two geckos (Gekkonidae: Gekkota) with female heterogamety,” Cytogenetic and Genome Research. In press.
  51. F. Gianfrancesco, R. Sanges, T. Esposito et al., “Differential divergence of three human pseudoautosomal genes and their mouse homologs: Implications for sex chromosome evolution,” Genome Research, vol. 11, no. 12, pp. 2095–2100, 2001. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Pokorná, L. Kratochvíl, and E. Kejnovský, “Microsatellite distribution on sex chromosomes at different stages of heteromorphism and heterochromatinization in two lizard species (Squamata: eublepharidae: coleonyx elegans and lacertidae: eremias velox),” BMC Genetics, vol. 12, article 90, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. Z. Kubat, R. Hobza, B. Vyskot, and E. Kejnovsky, “Microsatellite accumulation on the Y chromosome in Silene latifolia,” Genome, vol. 51, no. 5, pp. 350–356, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. J. Santos, L. Serra, E. Solé, and M. Pascual, “FISH mapping of microsatellite loci from drosophila subobscura and its comparison to related species,” Chromosome Research, vol. 18, no. 2, pp. 213–226, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. R. Bergero, D. Charlesworth, D. A. Filatov, and R. C. Moore, “Defining regions and rearrangements of the Silene latifolia Y chromosome,” Genetics, vol. 178, no. 4, pp. 2045–2053, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Iwase, Y. Satta, Y. Hirai, H. Hirai, H. Imai, and N. Takahata, “The amelogenin loci span an ancient pseudoautosomal boundary in diverse mammalian species,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 9, pp. 5258–5263, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. G. Marais and N. Galtier, “Sex chromosomes: how X-Y recombination stops,” Current Biology, vol. 13, no. 16, pp. R641–R643, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. J. A. Ross and C. L. Peichel, “Molecular cytogenetic evidence of rearrangements on the Y chromosome of the threespine stickleback fish,” Genetics, vol. 179, no. 4, pp. 2173–2182, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. R. Gorelick, “Evolution of dioecy and sex chromosomes via methylation driving Muller's ratchet,” Biological Journal of the Linnean Society, vol. 80, no. 2, pp. 353–368, 2003. View at Publisher · View at Google Scholar · View at Scopus
  60. E. Jablonka and M. J. Lamb, “The evolution of heteromorphic sex chromosomes,” Biological Reviews of the Cambridge Philosophical Society, vol. 65, no. 3, pp. 249–276, 1990. View at Publisher · View at Google Scholar · View at Scopus
  61. E. Jablonka, “The evolution of the peculiarities of mammalian sex chromosomes: an epigenetic view,” Bioessays, vol. 26, no. 12, pp. 1327–1332, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Suda, Y. Uno, Y. Mori, Y. Matsuda, and M. Nakamura, “Molecular cytogenetic characterization of telomere-specific repetitive DNA sequences in Rana rugosa,” Journal of Experimental Zoology A: Ecological Genetics and Physiology, vol. 315, no. 4, pp. 222–231, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. M. J. Young, D. O'Meally, S. D. Sarre, A. Georges, and T. Ezaz, “Molecular cytogenetic map of the central bearded dragon, Pogona vitticeps (Squamata: Agamidae),” Chromosome Research, vol. 21, no. 4, pp. 361–374, 2013. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Kawai, C. Nishida-Umehara, J. Ishijima, Y. Tsuda, H. Ota, and Y. Matsuda, “Different origins of bird and reptile sex chromosomes inferred from comparative mapping of chicken Z-linked genes,” Cytogenetic and Genome Research, vol. 117, no. 1–4, pp. 92–102, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Tone, Y. Sakaki, T. Hashiguchi, and S. Mizuno, “Genus specificity and extensive methylation of the W chromosome-specific repetitive DNA sequences from the domestic fowl, Gallus gallus domesticus,” Chromosoma, vol. 89, no. 3, pp. 228–237, 1984. View at Publisher · View at Google Scholar · View at Scopus
  66. P. P. Rabenold, W. H. Piper, M. D. Decker, and D. J. Minchella, “Polymorphic minisatellite amplified on avian W chromosome,” Genome, vol. 34, no. 3, pp. 489–493, 1991. View at Publisher · View at Google Scholar · View at Scopus
  67. C. Y. Miyaki, O. Hanotte, A. Wajntal, and T. Burke, “Sex typing of Aratinga parrots using the human minisatellite probe 33.15,” Nucleic Acids Research, vol. 20, no. 19, pp. 5235–5236, 1992. View at Publisher · View at Google Scholar · View at Scopus
  68. M. E. Delany, T. M. Gessaro, K. L. Rodrigue, and L. M. Daniels, “Chromosomal mapping of chicken mega-telomere arrays to GGA9, 16, 28 and W using a cytogenomic approach,” Cytogenetic and Genome Research, vol. 117, no. 1–4, pp. 54–63, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. P. Forster, A. Röhl, P. Lünnemann et al., “A short tandem repeat-based phylogeny for the human Y chromosome,” The American Journal of Human Genetics, vol. 67, no. 1, pp. 182–196, 2000. View at Publisher · View at Google Scholar · View at Scopus
  70. A. J. Macdonald, N. Sankovic, S. D. Sarre et al., “Y chromosome microsatellite markers identified from the tammar wallaby (Macropus eugenii) and their amplification in three other macropod species,” Molecular Ecology Notes, vol. 6, no. 4, pp. 1202–1204, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. V. J. Murtagh, D. O'Meally, N. Sankovic et al., “Evolutionary history of novel genes on the tammar wallaby Y chromosome: implications for sex chromosome evolution,” Genome Research, vol. 22, no. 3, pp. 498–507, 2012. View at Publisher · View at Google Scholar · View at Scopus
  72. R. D. Kortschak, E. Tsend-Ayush, and F. Grützner, “Analysis of SINE and LINE repeat content of Y chromosomes in the platypus, Ornithorhynchus anatinus,” Reproduction, Fertility and Development, vol. 21, no. 8, pp. 964–975, 2009. View at Publisher · View at Google Scholar · View at Scopus
  73. D. Bachtrog, “Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration,” Nature Reviews Genetics, vol. 14, no. 2, pp. 113–124, 2013. View at Publisher · View at Google Scholar · View at Scopus
  74. A. B. Carvalho and A. G. Clark, “Y chromosome of D. pseudoobscura is not homologous to the ancestral Drosophila Y,” Science, vol. 307, no. 5706, pp. 108–110, 2005. View at Publisher · View at Google Scholar · View at Scopus
  75. Q. Zhou and D. Bachtrog, “Sex-specific adaptation drives early sex chromosome evolution in Drosophila,” Science, vol. 337, no. 6092, pp. 341–345, 2012. View at Publisher · View at Google Scholar · View at Scopus
  76. Q. Zhou, C. E. Ellison, V. B. Kaiser, A. A. Alekseyenko, A. A. Gorchakov, and D. Bachtrog, “The epigenome of evolving Drosophila neo-sex chromosomes: dosage compensation and heterochromatin formation,” PLoS Biology, vol. 11, no. 11, Article ID e1001711, 2013. View at Publisher · View at Google Scholar · View at Scopus
  77. D. Bachtrog, E. Hom, K. M. Wong, X. Maside, and P. de Jong, “Genomic degradation of a young Y chromosome in Drosophila miranda,” Genome Biology, vol. 9, no. 2, article R30, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. M. Steinemann and S. Steinemann, “Degenerating Y chromosome of Drosophila miranda: a trap for retrotransposons,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 16, pp. 7591–7595, 1992. View at Publisher · View at Google Scholar · View at Scopus
  79. L. Singh, I. F. Purdom, and K. W. Jones, “Satellite DNA and evolution of sex chromosomes,” Chromosoma, vol. 59, no. 1, pp. 43–62, 1976. View at Publisher · View at Google Scholar · View at Scopus
  80. J. Arnemann, S. Jakubiczka, J. Schmidtke, R. Schäfer, and J. T. Epplen, “Clustered GATA repeats (Bkm sequences) on the human Y chromosome,” Human Genetics, vol. 73, no. 4, pp. 301–303, 1986. View at Publisher · View at Google Scholar · View at Scopus
  81. K. W. Jones and L. Singh, “Conserved repeated DNA sequences in vertebrate sex chromosomes,” Human Genetics, vol. 58, no. 1, pp. 46–53, 1981. View at Google Scholar · View at Scopus
  82. I. Nanda, C. Deubelbeiss, M. Guttenbach, J. T. Epplen, and M. Schmid, “Heterogeneities in the distribution of (GACA)n simple repeats in the karyotypes of primates and mouse,” Human Genetics, vol. 85, no. 2, pp. 187–194, 1990. View at Publisher · View at Google Scholar · View at Scopus
  83. I. Nanda, H. Zischler, C. Epplen, M. Guttenbach, and M. Schmid, “Chromosomal organization of simple repeated DNA sequences used for DNA fingerprinting,” Electrophoresis, vol. 12, no. 2-3, pp. 193–203, 1991. View at Publisher · View at Google Scholar · View at Scopus
  84. D. O'Meally, H. R. Patel, R. Stiglec et al., “Non-homologous sex chromosomes of birds and snakes share repetitive sequences,” Chromosome Research, vol. 18, no. 7, pp. 787–800, 2010. View at Publisher · View at Google Scholar · View at Scopus
  85. L. Singh, I. F. Purdom, and K. W. Jones, “Conserved sex-chromosome-associated nucleotide sequences in eukaryotes,” Cold Spring Harbor Symposia on Quantitative Biology, vol. 45, part 2, pp. 805–814, 1981. View at Publisher · View at Google Scholar · View at Scopus
  86. C. Biémont and C. Vieira, “Genetics: junk DNA as an evolutionary force,” Nature, vol. 443, no. 7111, pp. 521–524, 2006. View at Publisher · View at Google Scholar · View at Scopus
  87. S. Ohno, “So much “junk” DNA in our genome,” Brookhaven Symposia in Biology, vol. 23, pp. 366–370, 1972. View at Google Scholar · View at Scopus
  88. N. Chen, D. W. Bellott, D. C. Page, and A. G. Clark, “Identification of avian W-linked contigs by short-read sequencing,” BMC Genomics, vol. 13, no. 1, article 183, 2012. View at Publisher · View at Google Scholar · View at Scopus
  89. J. M. J. Lepesant, C. Cosseau, J. Boissier et al., “Chromatin structural changes around satellite repeats on the female sex chromosome in Schistosoma mansoni and their possible role in sex chromosome emergence,” Genome Biology, vol. 13, no. 2, article R14, 2012. View at Publisher · View at Google Scholar · View at Scopus
  90. T. B. Sackton and D. L. Hartl, “Meta-analysis reveals that genes regulated by the Y chromosome in Drosophila melanogaster are preferentially localized to repressive chromatin,” Genome Biology and Evolution, vol. 5, no. 1, pp. 255–266, 2013. View at Publisher · View at Google Scholar · View at Scopus
  91. P. P. Jiang, D. L. Hartl, and B. Lemos, “Y not a dead end: epistatic interactions between Y-linked regulatory polymorphisms and genetic background affect global gene expression in Drosophila melanogaster,” Genetics, vol. 186, no. 1, pp. 109–118, 2010. View at Publisher · View at Google Scholar · View at Scopus
  92. B. Lemos, L. O. Araripe, and D. L. Hartl, “Polymorphic Y chromosomes harbor cryptic variation with manifold functional consequences,” Science, vol. 319, no. 5859, pp. 91–93, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. B. Lemos, A. T. Branco, and D. L. Hartl, “Epigenetic effects of polymorphic Y chromosomes modulate chromatin components, immune response, and sexual conflict,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 36, pp. 15826–15831, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. T. B. Sackton, H. Montenegro, D. L. Hartl, and B. Lemos, “Interspecific Y chromosome introgressions disrupt testis-specific gene expression and male reproductive phenotypes in Drosophila,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 41, pp. 17046–17051, 2011. View at Publisher · View at Google Scholar · View at Scopus
  95. J. H. Malone and B. Oliver, “The sex chromosome that refused to die,” BioEssays, vol. 30, no. 5, pp. 409–411, 2008. View at Publisher · View at Google Scholar · View at Scopus
  96. W. R. Rice and U. Friberg, “Genetics: Functionally degenerate - Y not so?” Science, vol. 319, no. 5859, pp. 42–43, 2008. View at Publisher · View at Google Scholar · View at Scopus
  97. J. Zhou, T. B. Sackton, L. Martinsen, B. Lemos, T. H. Eickbush, and D. L. Hartl, “Y chromosome mediates ribosomal DNA silencing and modulates the chromatin state in Drosophila,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 25, pp. 9941–9946, 2012. View at Publisher · View at Google Scholar · View at Scopus
  98. R. Piergentili, “Multiple roles of the Y chromosome in the biology of Drosophila melanogaster,” TheScientificWorldJournal, vol. 10, pp. 1749–1767, 2010. View at Publisher · View at Google Scholar · View at Scopus
  99. L. K. Case, E. H. Wall, J. A. Dragon et al., “The y chromosome as a regulatory element shaping immune cell transcriptomes and susceptibility to autoimmune disease,” Genome Research, vol. 23, no. 9, pp. 1474–1485, 2013. View at Publisher · View at Google Scholar · View at Scopus
  100. N. P. Singh, S. R. Madabhushi, S. Srivastava et al., “Epigenetic profile of the euchromatic region of human y chromosome,” Nucleic Acids Research, vol. 39, no. 9, pp. 3594–3606, 2011. View at Publisher · View at Google Scholar · View at Scopus
  101. P. Priyadarshini, B. S. Murthy, J. Nagaraju, and L. Singh, “A GATA-binding protein expressed predominantly in the pupal ovary of the silkworm, Bombyx mori,” Insect Biochemistry and Molecular Biology, vol. 33, no. 2, pp. 185–195, 2003. View at Publisher · View at Google Scholar · View at Scopus
  102. L. Singh, R. Wadhwa, S. Naidu, R. Nagaraj, and M. Ganesan, “Sex- and tissue-specific Bkm(GATA)-binding protein in the germ cells of heterogametic sex,” Journal of Biological Chemistry, vol. 269, no. 41, pp. 25321–25327, 1994. View at Google Scholar · View at Scopus
  103. S. Subramanian, R. K. Mishra, and L. Singh, “Genome-wide analysis of Bkm sequences (GATA repeats): Predominant association with sex chromosomes and potential role in higher order chromatin organization and function,” Bioinformatics, vol. 19, no. 6, pp. 681–685, 2003. View at Publisher · View at Google Scholar · View at Scopus
  104. R. P. Kumar, J. Krishnan, N. Pratap Singh, L. Singh, and R. K. Mishra, “GATA simple sequence repeats function as enhancer blocker boundaries,” Nature Communications, vol. 4, article 1844, 2013. View at Publisher · View at Google Scholar · View at Scopus