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Multiple copies of SRY on the large Y chromosome of the Okinawa spiny rat, Tokudaia muenninki

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Abstract

The Okinawa spiny rat, Tokudaia muenninki, is the only species with a Y chromosome in the genus Tokudaia. Its phylogenic relationship with two XO/XO species, Tokudaia osimensis and Tokudaia tokunoshimensis, lacking a Y chromosome and the mammalian sex-determining gene SRY, is unknown. Furthermore, there has been little cytogenetic analysis of the sex chromosomes in T. muenninki. Therefore, we constructed molecular phylogenetic trees with nucleotide sequences of cyt b, RAG1, and IRBP. All trees strongly supported that T. muenninki was the first to diverge from the Tokudaia ancestor, indicating that loss of the Y chromosome and SRY occurred in the common ancestor of the two XO/XO species after T. muenninki diverged. We found that the X and Y chromosomes of T. muenninki consisted of large euchromatic and heterochromatic regions by conducting G- and C-banding analyses. PCR, Southern blotting, and FISH revealed that T. muenninki males had multiple SRY copies on the long arm of the Y chromosome. At least three of 24 SRY sequences contained a complete open reading frame (ORF). A species-specific substitution from alanine to serine was found in all copies at the DNA-binding surface within the HMG-box, suggesting that it occurred in an original SRY.

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Abbreviations

BSG:

Barium hydroxide/saline/Giemsa

DSD:

Disorders of sexual development

FISH:

Fluorescence in situ hybridization

GTG:

G-banding by Trypsin using Giemsa

HMG:

High-mobility group

IHB:

Intercalary heterochromatin block

L1:

Long interspersed nucleotide element 1

LTR:

Long terminal repeat

ML:

Maximum-likelihood

MP:

Maximum-parsimony

MYA:

Million years ago

NJ:

Neighbor-joining

ORF:

Open reading frame

SDS:

Sodium dodecyl sulfate

SSC:

Saline sodium citrate

TES:

Testis-specific enhancer of Sox9

UTR:

Untranslated region

References

  • Arakawa Y, Nishida-Umehara C, Matsuda Y, Sutou S, Suzuki H (2002) X-chromosomal localization of mammalian Y-linked genes in two XO species of the Ryukyu spiny rat. Cytogenet Genome Res 99:303–309

    Article  CAS  PubMed  Google Scholar 

  • Bergstrom D, Young M, Albrecht K, Eicher E (2000) Related function of mouse SOX3, SOX9, and SRY HMG domains assayed by male sex determination. Genesis 28:111–124

    Article  CAS  PubMed  Google Scholar 

  • Bianchi NO, Bianchi MS, Bailliet G, de la Chapelle A (1993) Characterization and sequencing of the sex determining region Y gene (Sry) in Akodon (Cricetidae) species with sex reversed females. Chromosoma 102:389–395

    Article  CAS  PubMed  Google Scholar 

  • Bullejos M, Sánchez A, Burgos M, Hera C, Jiménez R, Diaz de la Guardia R (1997) Multiple, polymorphic copies of SRY in both males and females of the vole Microtus cabrerae. Cytogenet Cell Genet 79:167–171

    Article  CAS  PubMed  Google Scholar 

  • Bullejos M, Sánchez A, Burgos M, Jiménez R, Diaz de la Guardia R (1999) Multiple mono- and polymorphic Y-linked copies of the SRY HMG-box in Microtidae. Cytogenet Cell Genet 86:46–50

    Article  CAS  PubMed  Google Scholar 

  • Deuve JL, Bennett NC, O'Brien PCM et al (2006) Complex evolution of X and Y autosomal translocations in the giant mole-rat, Cryptomys mechowi (Bathyergidae). Chromosome Res 14:681–691

    Article  CAS  PubMed  Google Scholar 

  • Dobigny G, Ozouf-Costaz C, Bonillo C, Volobouev V (2004) Viability of X-autosome translocations in mammals: an epigenomic hypothesis from a rodent case-study. Chromosoma 113:34–41

    Article  CAS  PubMed  Google Scholar 

  • Endo H, Tsuchiya K (2006) A new species of Ryukyu spiny rat, Tokudaia (Muridae: Rodentia), from Tokunoshima Island, Kagoshima Prefecture, Japan. Mamm study 31:47–57

    Article  Google Scholar 

  • Graves JAM (1995) The origin and function of the mammalian Y chromosome and Y-borne genes—an evolving understanding. BioEssays 17:311–320

    Article  CAS  PubMed  Google Scholar 

  • Honda T, Suzuki H, Itoh M (1977) An unusual sex chromosome constitution found in the Amami spinous country-rat, Tokudaia osimensis osimensis. Jpn J Genet 52:247–249

    Article  Google Scholar 

  • Honda T, Suzuki H, Itoh M, Hayashi K (1978) Karyotypical differences of the Amami spinous country-rats, Tokudaia osimensis osimensis obtained from two neighbouring islands. Jpn J Genet 53:297–299

    Article  Google Scholar 

  • Kamachi Y, Uchikawa M, Kondoh H (2000) Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet 16:182–187

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi T, Yamada F, Hashimoto T et al (2007) Exceptional minute sex-specific region in the X0 mammal, Ryukyu spiny rat. Chromosome Res 15:175–187

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi T, Yamada F, Hashimoto T et al (2008) Centromere repositioning in the X chromosome of XO/XO mammals, Ryukyu spiny rat. Chromosome Res 16:587–593

    Article  CAS  PubMed  Google Scholar 

  • Lundrigan BL, Tucker PK (1997) Evidence for multiple functional copies of the male sex-determining locus, Sry, in African murine rodents. J Mol Evol 45:60–65

    Article  CAS  PubMed  Google Scholar 

  • Marchal JA, Acosta MJ, Bullejos M, Diaz de la Guardia R, Sánchez A (2008) Origin and spread of the SRY gene on the X and Y chromosomes of the rodent Microtus cabrerae: role of L1 elements. Genomics 91:142–151

    Article  CAS  PubMed  Google Scholar 

  • Matsuda Y, Chapman VM (1995) Application of fluorescence in situ hybridization in genome analysis of the mouse. Electrophoresis 16:261–272

    Article  CAS  PubMed  Google Scholar 

  • Matsuda Y, Harada Y-N, Natsuume-Sakai S et al (1992) Location of the mouse complement factor H gene (cfh) by FISH analysis and replication R-banding. Cytogenet Cell Genet 61:282–285

    Article  CAS  PubMed  Google Scholar 

  • Michaux JR, Chevret P, Filippucci MG, Macholan M (2002) Phylogeny of the genus Apodemus with a special emphasis on the subgenus Sylvaemus using the nuclear IRBP gene and two mitochondrial markers: cytochrome b and 12 S rRNA. Mol Phylogenet Evol 23:123–136

    Article  CAS  PubMed  Google Scholar 

  • Murphy EC, Zhurkin VB, Louis JM, Cornilescu G, Clore GM (2001) Structural basis for SRY-dependent 46-X, Y sex reversal: modulation of DNA bending by a naturally occurring point mutation. J Mol Biol 312:481–499

    Article  CAS  PubMed  Google Scholar 

  • Nagamine CM (1994) The testis-determining gene, SRY, exists in multiple copies in Old World rodents. Genet Res 64:151–159

    Article  CAS  PubMed  Google Scholar 

  • Phillips NB, Nikolskaya T, Jancso-Radek A et al (2004) Sry-Directed Sex Reversal in Transgenic Mice Is Robust with Respect to Enhanced DNA Bending: Comparison of Human and Murine HMG-boxes. Biochemistry 43:7066–7081

    Article  CAS  PubMed  Google Scholar 

  • Polanco JC, Wilhelm D, Davidson TL, Knight D, Koopman P (2010) Sox10 gain-of-function causes XX sex reversal in mice: implications for human 22q-linked disorders of sex development. Hum Mol Genet 19:506–516

    Article  CAS  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Rowe KC, Reno ML, Richmond DM, Adkins RM, Steppan SJ (2008) Pliocene colonization and adaptive radiations in Australia and New Guinea (Sahul): Multilocus systematics of the old endemic rodents (Muroidea: Murinae). Mol Phylogenet Evol 47:84–101

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sato JJ, Suzuki H (2004) Phylogenetic relationships and divergence times of the genus Tokudaia within Murinae (Muridae; Rodentia) inferred from the nucleotide sequences encoding the Cytb gene, RAG1, and IRBP. Can J Zool 82:1343–1351

    Article  CAS  Google Scholar 

  • Sato JJ, Hosoda T, Wolsan M, Suzuki H (2004) Molecular Phylogeny of Arctoids (Mammalia: Carnivora) with Emphasis on Phylogenetic and Taxonomic Positions of the Ferret-badgers and Skunks. Zool Sci 21:111–118

    Article  CAS  PubMed  Google Scholar 

  • Seabright M (1971) A rapid banding technique for human chromosomes. Lancet 2:971–972

    Article  CAS  PubMed  Google Scholar 

  • Sekido R, Lovell-Badge R (2008) Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453:930–934

    Article  CAS  PubMed  Google Scholar 

  • Soullier S, Hanni C, Catzeflis F, Berta P, Laudet V (1998) Male sex determination in the spiny rat Tokudaia osimensis (Rodentia: Muridae) is not Sry dependent. Mamm Genome 9:590–592

    Article  CAS  PubMed  Google Scholar 

  • Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306

    Article  CAS  PubMed  Google Scholar 

  • Sutou S, Mitsui Y, Tsuchiya K (2001) Sex determination without the Y chromosome in two Japanese rodents Tokudaia osimensis osimensis and Tokudaia osimensis spp. Mamm Genome 12:17–21

    Article  CAS  PubMed  Google Scholar 

  • Suzuki H, Iwasa MA, Ishii N, Nagaoka H, Tsuchiya K (1999) The genetic status of two insular populations of the endemic spiny rat Tokudaia osimensis (Rodentia, Muridae) of the Ryukyu Islands, Japan. Mamm Study 24:43–50

    Article  Google Scholar 

  • Suzuki H, Tsuchiya K, Takezaki N (2000) A molecular phylogenetic framework for the Ryukyu endemic rodents Tokudaia osimensis and Diplothrix legata. Mol Phylogenet Evol 15:15–24

    Article  CAS  PubMed  Google Scholar 

  • Suzuki H, Sato JJ, Tsuchiya K et al (2003) Molecular phylogeny of wood mice (Apodemus, Muridae) in East Asia. Biol J Linn Soc 80:469–481

    Article  Google Scholar 

  • Swofford DL (2001) PAUP*: Phylogenetic analysis using parsimony (*and other methods). Version 4.0 beta version. Sinauer Associates, Sunderland, Mass

  • Tsuchiya K, Wakana S, Suzuki H, Hattori S, Hayashi Y (1989) Taxonomic study of Tokudaia (Rodentia: Muridae): I. Genetic differentiation. Memoirs Nat Sci Museum, Tokyo 22:227–234

    Google Scholar 

  • Turner ME, Martin C, Martins AS et al (2007) Genomic and expression analysis of multiple Sry loci from a single Rattus norvegicus Y chromosome. BMC Genet 8:11

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Werner MH, Huth JR, Gronenborn AM, Clore GM (1995) Molecular basis of human 46X, Y sex reversal revealed from the three-dimensional solution structure of the human SRY-DNA complex. Cell 81:705–714

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm D, Palmer S, Koopman P (2007) Sex determination and gonadal development in mammals. Physiol Rev 87:1–28

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank C. Nishida-Umehara and K. Matsubara for help with cell culturing and chromosome banding and Y. Miyake, N. Kotaka, and S. Abe for their efforts in capturing the animals. This work was supported by a Grant-in-aid for Scientific Research (No. 16086201) from the Ministry of Education, Culture, Sports, Science and Technology, Japan, the Global Environment Research Fund F-3 (for FY) from the Ministry of the Environment, Japan, a grant from the Sumitomo foundation, Japan, and a grant from Hokkaido University, Japan.

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Authors and Affiliations

  1. Graduate School of Life Science, Hokkaido University, Kita 10 Nishi 8, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan

    Chie Murata & Asato Kuroiwa

  2. Forestry and Forest Products Research Institute, Nagaikyutaro 68, Momoyama, Kyoto, 612-0855, Japan

    Fumio Yamada

  3. Yachiyo Engineering Co., Ltd., Kokuba Bldg. 9f, 3-21-1, kumoji, Naha, Okinawa, 900-0015, Japan

    Norihiro Kawauchi

  4. Laboratory of Animal Genetics, Department of Applied Molecular Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8601, Japan

    Yoichi Matsuda

  5. Laboratory of Animal Cytogenetics, Faculty of Science, Hokkaido University, Kita 10 Nishi 8, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan

    Asato Kuroiwa

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  1. Chie Murata
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  2. Fumio Yamada
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  4. Yoichi Matsuda
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Correspondence to Asato Kuroiwa.

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Responsible Editor: Fengtang Yang.

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Supplementary Figure S1

Alignment of 24 different sequences containing the full-length ORF of SRY with partial 5' UTR and 3' UTR of T. muenninki. Identical residues are indicated by dots (.). The start codons and the stop codons are colored dark gray and light gray, respectively. The HMG-box is underlined. The sites of insertion/deletion are indicated by (-). (PDF 80 kb)

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Murata, C., Yamada, F., Kawauchi, N. et al. Multiple copies of SRY on the large Y chromosome of the Okinawa spiny rat, Tokudaia muenninki . Chromosome Res 18, 623–634 (2010). https://doi.org/10.1007/s10577-010-9142-y

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