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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

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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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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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