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, 9 (6), R98

Neo-sex Chromosomes in the Black Muntjac Recapitulate Incipient Evolution of Mammalian Sex Chromosomes

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Neo-sex Chromosomes in the Black Muntjac Recapitulate Incipient Evolution of Mammalian Sex Chromosomes

Qi Zhou et al. Genome Biol.

Abstract

Background: The regular mammalian X and Y chromosomes diverged from each other at least 166 to 148 million years ago, leaving few traces of their early evolution, including degeneration of the Y chromosome and evolution of dosage compensation.

Results: We studied the intriguing case of black muntjac, in which a recent X-autosome fusion and a subsequent large autosomal inversion within just the past 0.5 million years have led to inheritance patterns identical to the traditional X-Y (neo-sex chromosomes). We compared patterns of genome evolution in 35-kilobase noncoding regions and 23 gene pairs on the homologous neo-sex chromosomes. We found that neo-Y alleles have accumulated more mutations, comprising a wide variety of mutation types, which indicates cessation of recombination and is consistent with an ongoing neo-Y degeneration process. Putative deleterious mutations were observed in coding regions of eight investigated genes as well as cis-regulatory regions of two housekeeping genes. In vivo assays characterized a neo-Y insertion in the promoter of the CLTC gene that causes a significant reduction in allelic expression. A neo-Y-linked deletion in the 3'-untranslated region of gene SNX22 abolished a microRNA target site. Finally, expression analyses revealed complex patterns of expression divergence between neo-Y and neo-X alleles.

Conclusion: The nascent neo-sex chromosome system of black muntjacs is a valuable model in which to study the evolution of sex chromosomes in mammals. Our results illustrate the degeneration scenarios in various genomic regions. Of particular importance, we report--for the first time--that regulatory mutations were probably able to accelerate the degeneration process of Y and contribute to further evolution of dosage compensation.

Figures

Figure 1
Figure 1
Neo-sex chromosomes of Muntiacus crinifrons. (a) Paring patterns in male and female black muntjacs during meiosis. The black areas on chromosomes represent homosynapsis regions, whereas gray areas represent heterosynapsis regions. Cross lines between chromosomes represent homologous recombination. A pentavalent involving five chromosomes will form during meiosis of male black muntjacs, whereas such structures are absent in female black muntjac. (b) Inversion on the neo-Y chromosome revealed by fluorescence in situ hybridization using two Indian muntjac bacterial artificial chromosome (BAC) clones, 06G7 (green) and 07B3 (red), as probes.
Figure 2
Figure 2
Dendrogram constructed using noncoding sequences of neo-Y and neo-X fragments. A total of 35.1-kilobase noncoding sequences of neo-Y and neo-X alleles in the black muntjac and the orthologous sequences in the Indian muntjac as the outgroup were used to construct the dentrogram. 'BM' stands for 'male black muntjac'; 'IM' stands for 'Indian muntjac'; '1'and '2' represent the two male black muntjac individuals separately. (a) Tree constructed by neighbor-joining method. Branch lengths calculated using Kimura's two-parameter method are shown above the corresponding branches. (b) Tree constructed by maximum likelihood method. Branch lengths calculated by baseml in PAML package using 'HKY85' method were shown above the corresponding branches.
Figure 3
Figure 3
Mutation in the promoter of CLTC gene severely causes downregulation of the neo-Y copy. Dual-reporter assay of promoter activities of CLTC. Standard error among triplicates was shown on the bar.
Figure 4
Figure 4
Expression divergences between nine neo-Y and neo-X gene pairs. All expression assays were done in duplicate and double checked in both male individuals. Mean expression ratios of neo-Y to neo-X are shown. The genes are arranged following the order from the centromere to the distal region of the 1p+4 chromosome.

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