Evolution from XIST-independent to XIST-controlled X-chromosome inactivation: epigenetic modifications in distantly related mammals

X chromosome inactivation (XCI) is the transcriptional silencing of one X in female mammals, balancing expression of X genes between females (XX) and males (XY). In placental mammals non-coding XIST RNA triggers silencing of one X (Xi) and recruits a characteristic suite of epigenetic modifications,...

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Bibliographic Details
Published in:PloS one 2011-04, Vol.6 (4), p.e19040-e19040
Main Authors: Chaumeil, Julie, Waters, Paul D, Koina, Edda, Gilbert, Clément, Robinson, Terence J, Graves, Jennifer A Marshall
Format: Article
Language:English
Subjects:
Analysis
Animals
Antibodies
Biology
Cell cycle
Chromatin
Chromosomes
Deactivation
DNA methylation
Epigenesis, Genetic
Epigenetic inheritance
Eukaryotes
Evolution
Evolution, Molecular
Evolutionary biology
Evolutionary genetics
Female
Females
Fluorescent Antibody Technique
Gene expression
Gene silencing
Genes
Genomics
Heterochromatin
Heterochromatin - metabolism
Histones - metabolism
Humans
Immunofluorescence
Inactivation
Life Sciences
Lysine - metabolism
Male
Males
Mammals
Mammals - genetics
Marsupialia - genetics
Marsupials
Methylation
Mice
Models, Genetic
Non-coding RNA
Nuclei
Phylogeny
Placenta
Recruitment
Ribonucleic acid
RNA
RNA, Long Noncoding
RNA, Untranslated - genetics
RNA-mediated interference
Stability
Stem cells
Territory
Transcription (Genetics)
Transcription, Genetic
X Chromosome
X Chromosome Inactivation - genetics
X-chromosome inactivation
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Summary:X chromosome inactivation (XCI) is the transcriptional silencing of one X in female mammals, balancing expression of X genes between females (XX) and males (XY). In placental mammals non-coding XIST RNA triggers silencing of one X (Xi) and recruits a characteristic suite of epigenetic modifications, including the histone mark H3K27me3. In marsupials, where XIST is missing, H3K27me3 association seems to have different degrees of stability, depending on cell-types and species. However, the complete suite of histone marks associated with the Xi and their stability throughout cell cycle remain a mystery, as does the evolution of an ancient mammal XCI system. Our extensive immunofluorescence analysis (using antibodies against specific histone modifications) in nuclei of mammals distantly related to human and mouse, revealed a general absence from the mammalian Xi territory of transcription machinery and histone modifications associated with active chromatin. Specific repressive modifications associated with XCI in human and mouse were also observed in elephant (a distantly related placental mammal), as was accumulation of XIST RNA. However, in two marsupial species the Xi either lacked these modifications (H4K20me1), or they were restricted to specific windows of the cell cycle (H3K27me3, H3K9me2). Surprisingly, the marsupial Xi was stably enriched for modifications associated with constitutive heterochromatin in all eukaryotes (H4K20me3, H3K9me3). We propose that marsupial XCI is comparable to a system that evolved in the common therian (marsupial and placental) ancestor. Silent chromatin of the early inactive X was exapted from neighbouring constitutive heterochromatin and, in early placental evolution, was augmented by the rise of XIST and the stable recruitment of specific histone modifications now classically associated with XCI.
ISSN:1932-6203
1932-6203
DOI:10.1371/journal.pone.0019040