The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation

Sex chromosomes are subject to sex-specific selective evolutionary forces 1 , 2 . One model predicts that genes with sex-biased expression should be enriched on the X chromosome 2 , 3 , 4 , 5 . In agreement with Rice's hypothesis 3 , spermatogonial genes are over-represented on the X chromosome...

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Published inNature genetics Vol. 36; no. 6; pp. 642 - 646
Main Authors Khil, Pavel P, Smirnova, Natalya A, Romanienko, Peter J, Camerini-Otero, R Daniel
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.06.2004
Nature Publishing Group
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Abstract Sex chromosomes are subject to sex-specific selective evolutionary forces 1 , 2 . One model predicts that genes with sex-biased expression should be enriched on the X chromosome 2 , 3 , 4 , 5 . In agreement with Rice's hypothesis 3 , spermatogonial genes are over-represented on the X chromosome of mice 6 and sex- and reproduction-related genes are over-represented on the human X chromosome 7 , 8 . Male-biased genes are under-represented on the X chromosome in worms and flies 9 , 10 , 11 , however. Here we show that mouse spermatogenesis genes are relatively under-represented on the X chromosome and female-biased genes are enriched on it. We used Spo11 −/− mice blocked in spermatogenesis early in meiosis 12 to evaluate the temporal pattern of gene expression in sperm development. Genes expressed before the Spo11 block are enriched on the X chromosome, whereas those expressed later in spermatogenesis are depleted. Inactivation of the X chromosome in male meiosis may be a universal driving force for X-chromosome demasculinization.
AbstractList Sex chromosomes are subject to sex-specific selective evolutionary forces. One model predicts that genes with sex-biased expression should be enriched on the X chromosome. In agreement with Rice's hypothesis, spermatogonial genes are over-represented on the X chromosome of mice and sex- and reproduction-related genes are over-represented on the human X chromosome. Male-biased genes are under-represented on the X chromosome in worms and flies, however. Here we show that mouse spermatogenesis genes are relatively under-represented on the X chromosome and female-biased genes are enriched on it. We used Spo11(-/-) mice blocked in spermatogenesis early in meiosis to evaluate the temporal pattern of gene expression in sperm development. Genes expressed before the Spo11 block are enriched on the X chromosome, whereas those expressed later in spermatogenesis are depleted. Inactivation of the X chromosome in male meiosis may be a universal driving force for X-chromosome demasculinization.
Sex chromosomes are subject to sex-specific selective evolutionary forces. One model predicts that genes with sex-biased expression should be enriched on the X chromosome. In agreement with Rice's hypothesis, spermatogonial genes are over-represented on the X chromosome of mice and sex- and reproduction-related genes are over-represented on the human X chromosome. Male-biased genes are under-represented on the X chromosome in worms and flies, however. Here we show that mouse spermatogenesis genes are relatively under-represented on the X chromosome and female-biased genes are enriched on it. We used Spo11(-/-) mice blocked in spermatogenesis early in meiosis to evaluate the temporal pattern of gene expression in sperm development. Genes expressed before the Spo11 block are enriched on the X chromosome, whereas those expressed later in spermatogenesis are depleted. Inactivation of the X chromosome in male meiosis may be a universal driving force for X-chromosome demasculinization.Sex chromosomes are subject to sex-specific selective evolutionary forces. One model predicts that genes with sex-biased expression should be enriched on the X chromosome. In agreement with Rice's hypothesis, spermatogonial genes are over-represented on the X chromosome of mice and sex- and reproduction-related genes are over-represented on the human X chromosome. Male-biased genes are under-represented on the X chromosome in worms and flies, however. Here we show that mouse spermatogenesis genes are relatively under-represented on the X chromosome and female-biased genes are enriched on it. We used Spo11(-/-) mice blocked in spermatogenesis early in meiosis to evaluate the temporal pattern of gene expression in sperm development. Genes expressed before the Spo11 block are enriched on the X chromosome, whereas those expressed later in spermatogenesis are depleted. Inactivation of the X chromosome in male meiosis may be a universal driving force for X-chromosome demasculinization.
Sex chromosomes are subject to sex-specific selective evolutionary forces. One model predicts that genes with sex-biased expression should be enriched on the X chromosome. In agreement with Rice's hypothesis, spermatogonial genes are over-represented on the X chromosome of mice and sex- and reproduction-related genes are over-represented on the human X chromosome. Male-biased genes are under-represented on the X chromosome in worms and flies, however. Here we show that mouse spermatogenesis genes are relatively under-represented on the X chromosome and female-biased genes are enriched on it. We used Spo11 super(-/-) mice blocked in spermatogenesis early in meiosis to evaluate the temporal pattern of gene expression in sperm development. Genes expressed before the Spo11 block are enriched on the X chromosome, whereas those expressed later in spermatogenesis are depleted. Inactivation of the X chromosome in male meiosis may be a universal driving force for X-chromosome demasculinization.
Sex chromosomes are subject to sex-specific selective evolutionary forces 1 , 2 . One model predicts that genes with sex-biased expression should be enriched on the X chromosome 2 , 3 , 4 , 5 . In agreement with Rice's hypothesis 3 , spermatogonial genes are over-represented on the X chromosome of mice 6 and sex- and reproduction-related genes are over-represented on the human X chromosome 7 , 8 . Male-biased genes are under-represented on the X chromosome in worms and flies 9 , 10 , 11 , however. Here we show that mouse spermatogenesis genes are relatively under-represented on the X chromosome and female-biased genes are enriched on it. We used Spo11 −/− mice blocked in spermatogenesis early in meiosis 12 to evaluate the temporal pattern of gene expression in sperm development. Genes expressed before the Spo11 block are enriched on the X chromosome, whereas those expressed later in spermatogenesis are depleted. Inactivation of the X chromosome in male meiosis may be a universal driving force for X-chromosome demasculinization.
Audience Academic
Author Romanienko, Peter J
Smirnova, Natalya A
Camerini-Otero, R Daniel
Khil, Pavel P
Author_xml – sequence: 1
  givenname: Pavel P
  surname: Khil
  fullname: Khil, Pavel P
  organization: Genetics and Biochemistry Branch, NIDDK, National Institutes of Health
– sequence: 2
  givenname: Natalya A
  surname: Smirnova
  fullname: Smirnova, Natalya A
  organization: Genetics and Biochemistry Branch, NIDDK, National Institutes of Health
– sequence: 3
  givenname: Peter J
  surname: Romanienko
  fullname: Romanienko, Peter J
  organization: Genetics and Biochemistry Branch, NIDDK, National Institutes of Health, Developmental Biology Program, Mouse Genetics Core, Memorial Sloan-Kettering Cancer Center
– sequence: 4
  givenname: R Daniel
  surname: Camerini-Otero
  fullname: Camerini-Otero, R Daniel
  email: camerini@ncifcrf.gov
  organization: Genetics and Biochemistry Branch, NIDDK, National Institutes of Health
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https://www.ncbi.nlm.nih.gov/pubmed/15156144$$D View this record in MEDLINE/PubMed
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Mammalia
Gene
Mouse
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Selection
Rodentia
Sex chromosome
Meiosis
X-Chromosome
Inactivation
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Snippet Sex chromosomes are subject to sex-specific selective evolutionary forces 1 , 2 . One model predicts that genes with sex-biased expression should be enriched...
Sex chromosomes are subject to sex-specific selective evolutionary forces. One model predicts that genes with sex-biased expression should be enriched on the X...
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SubjectTerms Agriculture
Animal Genetics and Genomics
Animals
Biological and medical sciences
Biomedical and Life Sciences
Biomedicine
Cancer Research
Chromosomes
Classical genetics, quantitative genetics, hybrids
Datasets
Dosage Compensation, Genetic
Endodeoxyribonucleases
Esterases - deficiency
Esterases - genetics
Female
Females
Fundamental and applied biological sciences. Psychology
Gene Expression
Gene Function
Genetic aspects
Genetics of eukaryotes. Biological and molecular evolution
Genome
Human Genetics
Inactivation
letter
Male
Meiosis - genetics
Mice
Mice, Knockout
Models, Genetic
Ovaries
Physiological aspects
Pregnancy
Sex chromosomes
Spermatogenesis
Spermatogenesis - genetics
Testes
Testis
Vertebrata
X Chromosome - genetics
X chromosomes
Title The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation
URI https://link.springer.com/article/10.1038/ng1368
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