Neo-sex chromosomes in the black muntjac recapitulate incipient evolution of mammalian sex chromosomes

Qi Zhou, Jun Wang, Ling Huang, Wenhui Nie, Jinhuan Wang, Yan Liu, Xiangyi Zhao, Fengtang Yang, Wen Wang

Research output: Contribution to journalJournal articleResearchpeer-review

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.
Original languageEnglish
JournalGenome Biology
Volume9
Issue number6
Pages (from-to)R98
ISSN1465-6906
DOIs
Publication statusPublished - 1. Jan 2008

Fingerprint

Muntjacs
sex chromosomes
chromosome
Mutation
mutation
gene
Y chromosome
Alleles
genes
Nucleic Acid Regulatory Sequences
Essential Genes
allele
alleles
MicroRNAs
autosomes
Mammals
3' untranslated regions
X chromosome
dosage
microRNA

Keywords

  • Animals
  • Evolution, Molecular
  • Female
  • Male
  • Muntjacs
  • Mutation
  • Transcription, Genetic
  • X Chromosome
  • Y Chromosome

Cite this

Zhou, Qi ; Wang, Jun ; Huang, Ling ; Nie, Wenhui ; Wang, Jinhuan ; Liu, Yan ; Zhao, Xiangyi ; Yang, Fengtang ; Wang, Wen. / Neo-sex chromosomes in the black muntjac recapitulate incipient evolution of mammalian sex chromosomes. In: Genome Biology. 2008 ; Vol. 9, No. 6. pp. R98.
@article{73a47de0ee2a11dd84b0000ea68e967b,
title = "Neo-sex chromosomes in the black muntjac recapitulate incipient evolution of mammalian sex chromosomes",
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.",
keywords = "Animals, Evolution, Molecular, Female, Male, Muntjacs, Mutation, Transcription, Genetic, X Chromosome, Y Chromosome",
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Zhou, Q, Wang, J, Huang, L, Nie, W, Wang, J, Liu, Y, Zhao, X, Yang, F & Wang, W 2008, 'Neo-sex chromosomes in the black muntjac recapitulate incipient evolution of mammalian sex chromosomes', Genome Biology, vol. 9, no. 6, pp. R98. https://doi.org/10.1186/gb-2008-9-6-r98

Neo-sex chromosomes in the black muntjac recapitulate incipient evolution of mammalian sex chromosomes. / Zhou, Qi; Wang, Jun; Huang, Ling; Nie, Wenhui; Wang, Jinhuan; Liu, Yan; Zhao, Xiangyi; Yang, Fengtang; Wang, Wen.

In: Genome Biology, Vol. 9, No. 6, 01.01.2008, p. R98.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Neo-sex chromosomes in the black muntjac recapitulate incipient evolution of mammalian sex chromosomes

AU - Zhou, Qi

AU - Wang, Jun

AU - Huang, Ling

AU - Nie, Wenhui

AU - Wang, Jinhuan

AU - Liu, Yan

AU - Zhao, Xiangyi

AU - Yang, Fengtang

AU - Wang, Wen

PY - 2008/1/1

Y1 - 2008/1/1

N2 - 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.

AB - 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.

KW - Animals

KW - Evolution, Molecular

KW - Female

KW - Male

KW - Muntjacs

KW - Mutation

KW - Transcription, Genetic

KW - X Chromosome

KW - Y Chromosome

U2 - 10.1186/gb-2008-9-6-r98

DO - 10.1186/gb-2008-9-6-r98

M3 - Journal article

C2 - 18554412

VL - 9

SP - R98

JO - Genome Biology (Online Edition)

JF - Genome Biology (Online Edition)

SN - 1474-7596

IS - 6

ER -