Table of Contents
International Journal of Evolutionary Biology
Volume 2014, Article ID 873935, 10 pages
http://dx.doi.org/10.1155/2014/873935
Research Article

A Syntenic Region Conserved from Fish to Mammalian X Chromosome

1Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, College of Fisheries and Life Sciences, Shanghai Ocean University and Laboratory of Reproductive Biology, Ministry of Education, Huchenghuan Road 999, Shanghai 201306, China
2Laboratory of Reproduction, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan
3Laboratory of Molecular Reproductive Biology, School of Marine Sciences, Sun Yat-sen University, 135 Xingang West Road, Guangzhou, China
4Lab of Molecular Developmental Biology, Institute for Environmental Sciences, University of Shizuoka, Yada, Shizuoka 422-8526, Japan
5Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543
6South Ehime Fisheries Research Center, Institution for Collaborative Relations, Ehime University, 3 Bunkyo-cho, Matsuyama 790-8577, Japan

Received 23 June 2014; Revised 30 October 2014; Accepted 2 November 2014; Published 18 November 2014

Academic Editor: E. N. Trifonov

Copyright © 2014 Guijun Guan et al. 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. A. Cutting, J. Chue, and C. A. Smith, “Just how conserved is vertebrate sex determination?” Developmental Dynamics, vol. 242, no. 4, pp. 380–387, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. A. E. Quinn, A. Georges, S. D. Sarre, F. Guarino, T. Ezaz, and J. A. M. Graves, “Temperature sex reversal implies sex gene dosage in a reptile,” Science, vol. 316, no. 5823, p. 411, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. C. S. Raymond, C. E. Shamu, M. M. Shen et al., “Evidence for evolutionary conservation of sex-determining genes,” Nature, vol. 391, no. 6668, pp. 691–695, 1998. View at Publisher · View at Google Scholar · View at Scopus
  4. 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
  5. M. Kondo, A. Froschauer, A. Kitano et al., “Molecular cloning and characterization of DMRT genes from the medaka Oryzias latipes and the platyfish Xiphophorus maculatus,” Gene, vol. 295, no. 2, pp. 213–222, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Matsuda, Y. Nagahama, A. Shinomiya et al., “DMY is a Y-specific DM-domain gene required for male development in the medaka fish,” Nature, vol. 417, no. 6888, pp. 559–563, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. R. S. Hattori, Y. Murai, M. Oura et al., “A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 8, pp. 2955–2959, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. T. Kamiya, W. Kai, S. Tasumi et al., “A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger Pufferfish, Takifugu rubripes (Fugu),” PLoS Genetics, vol. 8, no. 7, Article ID e1002798, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. T. Myosho, H. Otake, H. Masuyama et al., “Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis,” Genetics, vol. 191, no. 1, pp. 163–170, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Yano, R. Guyomard, B. Nicol et al., “An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss,” Current Biology, vol. 22, no. 15, pp. 1423–1428, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. Y. Takehana, M. T. Matsuda, M. L. Myosho et al., “Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena,” Nature Communications, vol. 5, article 4157, 2014. View at Publisher · View at Google Scholar
  12. M. Schartl, “A comparative view on sex determination in medaka,” Mechanisms of Development, vol. 121, no. 7-8, pp. 639–645, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Cnaani, “The tilapias' chromosomes influencing sex determination,” Cytogenetic and Genome Research, vol. 141, no. 2-3, pp. 195–205, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. J. F. Baroiller, H. D'Cotta, E. Bezault, S. Wessels, and G. Hoerstgen-Schwark, “Tilapia sex determination: where temperature and genetics meet,” Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, vol. 153, no. 1, pp. 30–38, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. G. C. Mair, A. G. Scott, D. J. Penman, J. A. Beardmore, and D. O. F. Skibinski, “Sex determination in the genus Oreochromis,” Theoretical and Applied Genetics, vol. 82, no. 2, pp. 144–152, 1991. View at Publisher · View at Google Scholar · View at Scopus
  16. L. A. P. Carrasco, D. J. Penman, S. A. Villalobos, and N. Bromage, “The effects of oral administration with 17α-methyltestosterone on chromosomal synapsis in Oreochromis niloticus (Pisces, Cichlidae),” Mutation Research: Fundamental and Molecular Mechanisms of Mutagenesis, vol. 430, no. 1, pp. 87–98, 1999. View at Publisher · View at Google Scholar · View at Scopus
  17. S. C. Harvey, R. Campos-Ramos, D. D. Kennedy et al., “Karyotype evolution in tilapia: Mitotic and meiotic chromosome analysis of Oreochromis karongae and O. niloticus x O. karongae hybrids,” Genetica, vol. 115, no. 2, pp. 169–177, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. S. C. Harvey, J. Masabanda, L. A. P. Carrasco, N. R. Bromage, D. J. Penman, and D. K. Griffin, “Molecular-cytogenetic analysis reveals sequence differences between the sex chromosomes of Oreochromis niloticus: evidence for an early stage of sex-chromosome differentiation,” Cytogenetic and Genome Research, vol. 97, no. 1-2, pp. 76–80, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. M. T. Ezaz, S. C. Harvey, C. Boonphakdee, A. J. Teale, B. J. McAndrew, and D. J. Penman, “Isolation and physical mapping of sex-linked AFLP markers in Nile tilapia (Oreochromis niloticus L.),” Marine Biotechnology, vol. 6, no. 5, pp. 435–445, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. B.-Y. Lee, J.-P. Coutanceau, C. Ozouf-Costaz, H. D'Cotta, J.-F. Baroiller, and T. D. Kocher, “Genetic and physical mapping of sex-linked AFLP markers in nile tilapia (Oreochromis niloticus),” Marine Biotechnology, vol. 13, no. 3, pp. 557–562, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Wessels, R. A. Sharifi, L. M. Luehmann et al., “Allelic variant in the anti-mullerian hormone gene leads to autosomal and temperature-dependent sex reversal in a selected nile tilapia line,” PLoS ONE, vol. 9, no. 8, Article ID e104795, 2014. View at Publisher · View at Google Scholar
  22. G. Guan, T. Kobayashi, and Y. Nagahama, “Sexually dimorphic expression of two types of DM (Doublesex/Mab-3)-domain genes in a teleost fish, the Tilapia (Oreochromis niloticus),” Biochemical and Biophysical Research Communications, vol. 272, no. 3, pp. 662–666, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. J. N. Volff and M. Schartl, “Sex determination and sex chromosome evolution in the medaka, Oryzias latipes, and the platyfish, Xiphophorus maculatus,” Cytogenetic and Genome Research, vol. 99, no. 1–4, pp. 170–177, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Kondo, I. Nanda, U. Hornung et al., “Absence of the candidate male sex-determining gene dmrt1b(Y) of medaka from other fish species,” Current Biology, vol. 13, no. 5, pp. 416–420, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Nagahama, “Molecular mechanisms of sex determination and gonadal sex differentiation in fish,” Fish Physiology and Biochemistry, vol. 31, no. 2-3, pp. 105–109, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Ijiri, H. Kaneko, T. Kobayashi et al., “Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus,” Biology of Reproduction, vol. 78, no. 2, pp. 333–341, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. H. D'Cotta, A. Fostier, Y. Guiguen, M. Govoroun, and J.-F. Baroiller, “Aromatase plays a key role during normal and temperature-induced sex differentiation of tilapia Oreochromis niloticus,” Molecular Reproduction and Development, vol. 59, no. 3, pp. 265–276, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Kobayashi, H. Kajiura-Kobayashi, G. Guan, and Y. Nagahama, “Sexual dimorphic expression of DMRT1 and Sox9a during gonadal differentiation and hormone-induced sex reversal in the teleost fish nile tilapia (Oreochromis niloticus),” Developmental Dynamics, vol. 237, no. 1, pp. 297–306, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. X. Chang, T. Kobayashi, B. Senthilkumaran, H. Kobayashi-Kajura, C. C. Sudhakumari, and Y. Nagahama, “Two types of aromatase with different encoding genes, tissue distribution and developmental expression in Nile tilapia (Oreochromis niloticus),” General and Comparative Endocrinology, vol. 141, no. 2, pp. 101–115, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. S. C. Harvey, J. Y. Kwon, and D. J. Penman, “Physical mapping of the brain and ovarian aromatase genes in the Nile Tilapia, Oreochromis niloticus, by fluorescence in situ hybridization,” Animal Genetics, vol. 34, no. 1, pp. 62–64, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Kallioniemi, O.-P. Kallioniemi, D. Sudar et al., “Comparative genomic hybridization for molecular cytogenetic analysis of solid tumors,” Science, vol. 258, no. 5083, pp. 818–821, 1992. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Obara, S. Matsunaga, S. Nakao, and S. Kawano, “A plant Y chromosome-STS marker encoding a degenerate retrotransposon,” Genes and Genetic Systems, vol. 77, no. 6, pp. 393–398, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. P. Gebler, Ł. Wolko, and M. Knaflewski, “Identification of molecular markers for selection of supermale (YY) asparagus plants,” Journal of Applied Genetics, vol. 48, no. 2, pp. 129–131, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. W. Traut, K. Sahara, T. D. Otto, and F. Marec, “Molecular differentiation of sex chromosomes probed by comparative genomic hybridization,” Chromosoma, vol. 108, no. 3, pp. 173–180, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. M. S. Yi, Y. Q. Li, J. D. Liu, L. Zhou, Q. X. Yu, and J. F. Gui, “Molecular cytogenetic detection of paternal chromosome fragments in allogynogenetic gibel carp, Carassius auratus gibelio Bloch,” Chromosome Research, vol. 11, no. 7, pp. 665–671, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. B.-Y. Lee, D. J. Penman, and T. D. Kocher, “Identification of a sex-determining region in Nile tilapia (Oreochromis niloticus) using bulked segregant analysis,” Animal Genetics, vol. 34, no. 5, pp. 379–383, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. B.-Y. Lee, W.-J. Lee, J. T. Streelman et al., “A second-generation genetic linkage map of tilapia (Oreochromis spp.),” Genetics, vol. 170, no. 1, pp. 237–244, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. R. Guyomard, M. Boussaha, F. Krieg, C. Hervet, and E. Quillet, “A synthetic rainbow trout linkage map provides new insights into the salmonid whole genome duplication and the conservation of synteny among teleosts,” BMC Genetics, vol. 13, article 15, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. J. E. Mank, E. Axelsson, and H. Ellegren, “Fast-X on the Z: rapid evolution of sex-linked genes in birds,” Genome Research, vol. 17, no. 5, pp. 618–624, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. R. Campos-Ramos, S. C. Harvey, J. S. Masabanda et al., “Identification of putative sex chromosomes in the blue tilapia, Oreochromis aureus, through synaptonemal complex and fish analysis,” Genetica, vol. 111, no. 1–3, pp. 143–153, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. J. C. Mota-Velasco, I. A. Ferreira, M. B. Cioffi et al., “Characterisation of the chromosome fusions in Oreochromis karongae,” Chromosome Research, vol. 18, no. 5, pp. 575–586, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. B.-Y. Lee, G. Hulata, and T. D. Kocher, “Two unlinked loci controlling the sex of blue tilapia (Oreochromis aureus),” Heredity, vol. 92, no. 6, pp. 543–549, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Cnaani, B.-Y. Lee, N. Zilberman et al., “Genetics of sex determination in tilapiine species,” Sexual Development, vol. 2, no. 1, pp. 43–54, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Qvarnström and R. I. Bailey, “Speciation through evolution of sex-linked genes,” Heredity, vol. 102, no. 1, pp. 4–15, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. D. W. Bellott, H. Skaletsky, T. Pyntikova et al., “Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition,” Nature, vol. 466, no. 7306, pp. 612–616, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. J. A. Marshall 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
  47. F. Veyrunes, P. D. Waters, P. Miethke et al., “Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes,” Genome Research, vol. 18, no. 6, pp. 965–973, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Alonso and J. A. L. Armour, “Compound haplotypes at Xp11.23 and human population growth in Eurasia,” Annals of Human Genetics, vol. 68, no. 5, pp. 428–437, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. I. Nanda, M. Kondo, U. Hornung et al., “A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 18, pp. 11778–11783, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. I. Nanda, E. Zend-Ajusch, Z. Shan et al., “Conserved synteny between the chicken Z sex chromosome and human chromosome 9 includes the male regulatory gene DMRT1: a comparative (re)view on avian sex determination,” Cytogenetics and Cell Genetics, vol. 89, no. 1-2, pp. 67–78, 2000. View at Publisher · View at Google Scholar · View at Scopus
  51. F. Grutzner and J. A. Graves, “A platypus' eye view of the mammalian genome,” Current Opinion in Genetics and Development, vol. 14, no. 6, pp. 642–649, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. T. Ezaz, R. Stiglec, F. Veyrunes, and J. A. M. 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
  53. J. J. Smith and S. R. Voss, “Bird and mammal sex-chromosome orthologs map to the same autosomal region in a salamander (Ambystoma),” Genetics, vol. 177, no. 1, pp. 607–613, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. G. Hulata, G. Wohlfarth, and S. Rothbard, “Progeny-testing selection of tilapia broodstocks producing all-male hybrid progenies-preliminary results,” Aquaculture, vol. 33, no. 1–4, pp. 263–268, 1983. View at Publisher · View at Google Scholar · View at Scopus
  55. R. P. Phelps and T. J. Popma, “Sex reversal of tilapia,” in Tilapia Aquaculture in the Americas, vol. 2, pp. 34–59, 2000. View at Google Scholar
  56. F. Liu, F. Sun, J. Li et al., “A microsatellite-based linkage map of salt tolerant tilapia (Oreochromis mossambicus x Oreochromis spp.) and mapping of sex-determining loci,” BMC Genomics, vol. 14, no. 1, article 58, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. C. Palaiokostas, M. Bekaert, M. G. Q. Khan et al., “Mapping and validation of the major sex-determining region in Nile tilapia (Oreochromis niloticus L.) Using RAD sequencing,” PLoS ONE, vol. 8, no. 7, Article ID e68389, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Kumar and S. B. Hedges, “A molecular timescale for vertebrate evolution,” Nature, vol. 392, no. 6679, pp. 917–920, 1998. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Ruta, M. I. Coates, and D. L. Quicke, “Early tetrapod relationships revisited,” Biological Reviews of the Cambridge Philosophical Society, vol. 78, no. 2, pp. 251–345, 2003. View at Google Scholar