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Ancestral Y-linked genes were maintained by translocation to the X and Y chromosomes fused to an autosomal pair in the Okinawa spiny rat Tokudaia muenninki

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Abstract

Two species of the genus Tokudaia lack the Y chromosome and SRY, but several Y-linked genes have been rescued by translocation or transposition to other chromosomes. Tokudaia muenninki is the only species in the genus that maintains the Y owing to sex chromosome-autosome fusions. According to previous studies, many SRY pseudocopies and other Y-linked genes have evolved by excess duplication in this species. Using RNA-seq and RT-PCR, we found that ZFY, EIF2S3Y, TSPY, UTY, DDX3Y, USP9Y, and RBMY, but not UBA1Y, had high deduced amino acid sequence similarity and similar expression patterns with other rodents, suggesting that these genes were functional. Based on FISH and quantitative real-time PCR, all of the genes except for UTY and DDX3Y were amplified on the X and Y chromosomes with approximately 10–66 copies in the male genome. In a comparative analysis of the 372.4-kb BAC sequence and Y-linked gene transcripts from T. muenninki with the mouse Y genomic sequence, we observed that multiple-copy genes in the ancestral Y genome were nonfunctional, indicating that the gene functions were assumed by amplified copies. We also found a LTR sequence at the distal end of a SRY duplication unit, suggesting that unequal sister chromatid exchange mediated by retrotransposable elements could have been involved in SRY amplification. Our results revealed that the Y-linked genes were rescued from degeneration via translocations to other sex chromosomal regions and amplification events in T. muenninki.

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Abbreviations

BAC:

Bacterial artificial chromosome

FISH:

Fluorescent in situ hybridization

LINE:

Long interspersed element

LTR:

Long-terminal repeat

qPCR:

Quantitative real-time PCR

RACE:

Rapid amplification of cDNA ends

RT-PCR:

Reverse transcription PCR

TESCO:

The core region within testis-specific enhancer of SOX9

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Acknowledgments

The authors thank F. Yamada, T. Jogahara, C. Koshimoto, T. Mitani, and K. Nakata for their efforts in capturing the animals and the Fujii Memorial Institute of Medical Sciences, Tokushima University, for support with fluorescence microscopy. This work was supported by JSPS KAKENHI Grant Numbers 23870023 and 26870410.

Authors’ contributions

CM conceived of and designed the study, performed molecular and cytogenetic experiments and all data analysis, and drafted the manuscript. YK conducted RNA-seq. II participated in total RNA and BAC DNA extraction and commented on the manuscript. AK conceived of and designed the study and participated in drafting the manuscript. All authors read and approved of the final manuscript.

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Author notes

  1. Yoko Kuroki

    Present address: Division of Pediatric Disease Genomics, Department of Genome Medicine, National Research Institute for Child Health and Development, 2-10-1, Okura, Setagaya-ku, Tokyo, 157-8535, Japan

Authors and Affiliations

  1. Department of Human Genetics, Institute of Biomedical Sciences, Tokushima University Graduate School, 3-18-15 Kuramoto-cho, Tokushima, 770-8503, Japan

    Chie Murata & Issei Imoto

  2. RIKEN, Center for Integrative Medical Sciences, 1-7-22 Suehiro-cho, Tsurumi, Yokohama, Kanagawa, 230-0045, Japan

    Yoko Kuroki

  3. 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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Correspondence to Asato Kuroiwa.

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Responsible Editor: Tatsuo Fukagawa, Ph.D

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Figure S1

Alignment of the nucleotide and amino acid sequences of nine Y-linked genes between T. muenninki and other rodents. The coding region from the mRNA and/or genomic sequences of ZFY (a, b), UBA1Y (c, d), EIF2S3Y (e, f), TSPY (g, h), UTY (i, j), DDX3Y (k, l), USP9Y (m, n), RBMY (o, p), and SRY (q) in T. muenninki were compared with orthologous sequences in mouse, rat, T. osimensis, and/or A. sylvaticus. Identical residues are indicated by dots. TMU: T. muenninki. The deletion and the internal stop codon are colored in gray (a) and pink (m), respectively. Asterisks show the stop codon sites in the amino acid sequences (b, d, f, h, j, l, n, p). Single nucleotide and amino acid polymorphisms within T. muenninki transcripts of each gene are shown in red letters (e–h, m–p). Different nucleotide sites of genomic sequences from the mRNAs of T. muenninki are shown in blue letters (e, g, m, o). (q) The start codons and the stop codons are colored in blue. SRY25 is the genomic sequence observed upstream of EIF2S3Y in this study. SRY1–24 sequences of T. muenninki are reported by Murata et al. 2010, of which only three (SRY1–3) have the conserved coding sequences. The repeat sequence was partially skipped in the mouse (600 bp), and the skipped site is shown by double slashes. (PDF 30457 kb)

Figure S2

Neighbor-joining trees constructed with each X/Y gene sequence of T. muenninki and other rodents. Number above and below branches refer to bootstrap percentages. The values less than 70 % are not shown. TMU T. muenninki; MMU M.musculus; RNO R. norvegicus; ASY A. sylvaticus (GIF 26 kb)

High Resolution Image (TIF 2612 kb)

Figure S3

Chromosomal location of two X-linked genes in T. muenninki. A fluorescent in situ hybridization (FISH) analysis showed that ZFX (a, b) and UBA1 (c, d) are distributed on the middle and pericentromeric regions of Xq, respectively. The hybridization signals are indicated by arrowheads. R- (a, c) and G-banding (b, d) patterns are shown. The scale bars represent 10 μm. (GIF 209 kb)

High Resolution Image (TIF 4552 kb)

Figure S4

Nucleotide alignment of the accepter splicing site within intron 15 of DDX3Y between T. muenninki and mouse. The intronic sites are colored in gray for each species. Arrows show the boundary between an exon and intron. Asterisks show the identical sites between two sequences. (GIF 29 kb)

High Resolution Image (TIF 133 kb)

Figure S5

Nucleotide sequence alignment in the conserved upstream (a) and downstream (b) regions of SRY among T. muenninki, mouse, and rat. Identical residues are indicated by dots. The skipped site is shown by double slashes. TMU: T. muenninki. (PDF 14453 kb)

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Murata, C., Kuroki, Y., Imoto, I. et al. Ancestral Y-linked genes were maintained by translocation to the X and Y chromosomes fused to an autosomal pair in the Okinawa spiny rat Tokudaia muenninki . Chromosome Res 24, 407–419 (2016). https://doi.org/10.1007/s10577-016-9531-y

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