Paternal X inactivation does not correlate with X chromosome evolutionary strata in marsupials

BMC Evolutionary Biology

Paul D Waters¹  Shafagh A Waters¹  Claudia L Rodríguez-Delgado² 

[1] School of Biotechnology and Biomolecular Sciences, Faculty of Science, University of New South Wales, Sydney, NSW, Australia;Division of Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra 0200, ACT, Australia

关键词: Strata;    Evolution;    SNP;    RNA-seq;    Escape;    X chromosome;    Imprinting;    Marsupial;    X inactivation;   

Others  :  1121723
DOI  :  10.1186/s12862-014-0267-z

 received in 2014-08-19, accepted in 2014-12-11,  发布年份 2014

【 摘 要 】

Background

X chromosome inactivation is the transcriptional silencing of one X chromosome in the somatic cells of female mammals. In eutherian mammals (e.g. humans) one of the two X chromosomes is randomly chosen for silencing, with about 15% (usually in younger evolutionary strata of the X chromosome) of genes escaping this silencing. In contrast, in the distantly related marsupial mammals the paternally derived X is silenced, although not as completely as the eutherian X. A chromosome wide examination of X inactivation, using RNA-seq, was recently undertaken in grey short-tailed opossum (Monodelphis domestica) brain and extraembryonic tissues. However, no such study has been conduced in Australian marsupials, which diverged from their American cousins ~80 million years ago, leaving a large gap in our understanding of marsupial X inactivation.

Results

We used RNA-seq data from blood or liver of a family (mother, father and daughter) of tammar wallabies (Macropus eugenii), which in conjunction with available genome sequence from the mother and father, permitted genotyping of 42 expressed heterozygous SNPs on the daughter’s X. These 42 SNPs represented 34 X loci, of which 68% (23 of the 34) were confirmed as inactivated on the paternally derived X in the daughter’s liver; the remaining 11 X loci escaped inactivation. Seven of the wallaby loci sampled were part of the old X evolutionary stratum, of which three escaped inactivation. Three loci were classified as part of the newer X stratum, of which two escaped inactivation. A meta-analysis of previously published opossum X inactivation data revealed that 5 of 52 genes in the old X stratum escaped inactivation.

Conclusions

We demonstrate that chromosome wide inactivation of the paternal X is common to an Australian marsupial representative, but that there is more escape from inactivation than reported for opossum (32% v 14%). We also provide evidence that, unlike the human X chromosome, the location of loci within the oldest evolutionary stratum on the marsupial X does not correlate with their probability of escape from inactivation.

【 授权许可】

   
2014 Rodríguez-Delgado et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Muller HJ: A gene for the fourth chromosome of drosophila. J Exp Zool 1914, 17(3):325-336.
• [2]Pessia E, Makino T, Bailly-Bechet M, McLysagh A, Marias ABG: Mammalian X chromosome inactivation evolved as a dosage-compensation mechanism for dosage-sensitive genes on the X chromosome. Proc Natl Acad Sci U S A 2012, 109(14):5346-5351.
• [3]Ohno S: Sex Chromosomes and Sex Linked Genes. Springer, Berlin; 1967.
• [4]Lyon MF: Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 1961, 190:372-373.
• [5]Brown CJ, Ballabio A, Rupert JL, Lafreniere RG, Grompe M, Tonlorenzi R, Willard HF: A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 1991, 349(6304):38-44.
• [6]Heard E, Clerc P, Avner P: X-chromosome inactivation in mammals. Annu Rev Genet 1997, 31:571-610.
• [7]Carrel L, Willard HF: X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 2005, 434(7031):400-404.
• [8]Johnston CM, Lovell FL, Leongamornlert DA, Stranger BE, Dermitzakis ET, Ross MT: Large-scale population study of human cell lines indicates that dosage compensation is virtually complete. PLoS Genet 2008, 4(1):e9.
• [9]Wang X, Miller DC, Clark AG, Antczak DF: Random X inactivation in the mule and horse placenta. Genome Res 2012, 22(10):1855-1863.
• [10]Payer B, Lee JT: X chromosome dosage compensation: how mammals keep the balance. Annu Rev Genet 2008, 42:733-772.
• [11]de Mello JC M, de Araujo ES, Stabellini R, Fraga AM, de Souza JE, Sumita DR, Camargo AA, Pereira LV: Random X inactivation and extensive mosaicism in human placenta revealed by analysis of allele-specific gene expression along the X chromosome. PLoS One 2010, 5(6):e10947.
• [12]Okamoto I, Patrat C, Thepot D, Peynot N, Fauque P, Daniel N, Diabangouaya P, Wolf JP, Renard JP, Duranthon V, Heard E: Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development. Nature 2011, 472(7343):370-374.
• [13]Waters PD, Ruiz-Herrera A, Dobigny G, Garcia Caldes M, Robinson TJ: Sex chromosomes of basal placental mammals. Chromosoma 2007, 116(6):511-518.
• [14]Waters PD, Dobigny G, Pardini AT, Robinson TJ: LINE-1 distribution in Afrotheria and Xenarthra: implications for understanding the evolution of LINE-1 in eutherian genomes. Chromosoma 2004, 113(3):137-144.
• [15]Bell RJ, Lees GE, Murphy KE: X chromosome inactivation patterns in normal and X-linked hereditary nephropathy carrier dogs. Cytogenet Genome Res 2008, 122(1):37-40.
• [16]Graves JA, Watson JM: Mammalian sex chromosomes: evolution of organization and function. Chromosoma 1991, 101(2):63-68.
• [17]Cooper DW, Johnston PG, Vandeberg JL, Robinson ES: X-Chromosome Inactivation in Marsupials. Aust J Zool 1990, 37(2–4):411-417.
• [18]Mahadevaiah SK, Royo H, VandeBerg JL, McCarrey JR, Mackay S, Turner JM: Key features of the X inactivation process are conserved between marsupials and eutherians. Curr Biol: CB 2009, 19(17):1478-1484.
• [19]Chaumeil J, Waters PD, Koina E, Gilbert C, Robinson TJ, Graves JA: Evolution from XIST-independent to XIST-controlled X-chromosome inactivation: epigenetic modifications in distantly related mammals. PLoS One 2011, 6(4):e19040.
• [20]Rens W, Wallduck MS, Lovell FL, Ferguson-Smith MA, Ferguson-Smith AC: Epigenetic modifications on X chromosomes in marsupial and monotreme mammals and implications for evolution of dosage compensation. Proc Natl Acad Sci U S A 2010, 107(41):17657-17662.
• [21]Hore TA, Koina E, Wakefield MJ, Marshall Graves JA: The region homologous to the X-chromosome inactivation centre has been disrupted in marsupial and monotreme mammals. Chromosome Res 2007, 15(2):147-161.
• [22]Shevchenko AI, Zakharova IS, Elisaphenko EA, Kolesnikov NN, Whitehead S, Bird C, Ross M, Weidman JR, Jirtle RL, Karamysheva TV, Rubtsov NB, VandeBerg JL, Mazurok NA, Nesterova TB, Brockdorff N, Zakian SM: Genes flanking Xist in mouse and human are separated on the X chromosome in American marsupials. Chromosome Res 2007, 15(2):127-136.
• [23]Davidow LS, Breen M, Duke SE, Samollow PB, McCarrey JR, Lee JT: The search for a marsupial XIC reveals a break with vertebrate synteny. Chromosome Res 2007, 15(2):137-146.
• [24]Duret L, Chureau C, Samain S, Weissenbach J, Avner P: The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 2006, 312(5780):1653-1655.
• [25]Grant J, Mahadevaiah SK, Khil P, Sangrithi MN, Royo H, Duckworth J, McCarrey JR, VandeBerg JL, Renfree MB, Taylor W, Elgar G, Camerini-Otero RD, Gilchrist MJ, Turner JM: Rsx is a metatherian RNA with Xist-like properties in X-chromosome inactivation. Nature 2012, 487(7406):254-258.
• [26]Johnston PG, Sharman GB: Studies on metatherian sex chromosomes. I. Inheritance and inactivation of sex-linked allelic genes determining glucose-6-phosphate dehydrogenase variation in kangaroos. Aust J Biol Sci 1975, 28(5-6):567-574.
• [27]Samollow PB, Ford AL, VandeBerg JL: X-linked gene expression in the Virginia opossum: differences between the paternally derived Gpd and Pgk-A loci. Genetics 1987, 115(1):185-195.
• [28]Cooper DW, Edwards C, James E, Sharman GB, Vandeberg JL, Marshall Graves JA: Studies on metatherian sex chromosomes VI. A third state of an X-linked gene: partial activity for the paternally derived Pgk-A allele in cultured fibroblasts of Macropus giganteus and M. parryi. Aust J Biol Sci 1977, 30:431-443.
• [29]Cooper DW, Woolley PA, Maynes GM, Sherman FS, Poole WE: Studies on metatherian sex chromosomes. XII. Sex-linked inheritance and probable paternal X-inactivation of alpha-galactosidase A in Australian marsupials. Aust J Biol Sci 1983, 36(5–6):511-517.
• [30]Graves JA, Dawson GW: The relationship between position and expression of genes on the kangaroo X chromosome suggests a tissue-specific spread of inactivation from a single control site. Genet Res 1988, 51(2):103-109.
• [31]Wake N, Takagi N, Sasaki M: Non-random inactivation of X chromosome in the rat yolk sac. Nature 1976, 262(5569):580-581.
• [32]West JD, Papaioannou VE, Frels WI, Chapman VM: Preferential expression of the maternally derived X chromosome in extraembryonic tissues of the mouse. Basic Life Sci 1978, 12:361-377.
• [33]Dindot SV, Kent KC, Evers B, Loskutoff N, Womack J, Piedrahita JA: Conservation of genomic imprinting at the XIST, IGF2, and GTL2 loci in the bovine. Mamm Genome 2004, 15(12):966-974.
• [34]Wang X, Douglas KC, Vandeberg JL, Clark AG, Samollow PB: Chromosome-wide profiling of X-chromosome inactivation and epigenetic states in fetal brain and placenta of the opossum, Monodelphis domestica. Genome Res 2014, 24(1):70-83.
• [35]Yang F, Babak T, Shendure J, Disteche CM: Global survey of escape from X inactivation by RNA-sequencing in mouse. Genome Res 2010, 20(5):614-622.
• [36]Cortez D, Marin R, Toledo-Flores D, Froidevaux L, Liechti A, Waters PD, Grutzner F, Kaessmann H: Origins and functional evolution of Y chromosomes across mammals. Nature 2014, 508(7497):488-493.
• [37]Renfree MB, Papenfuss AT, Deakin JE, Lindsay J, Heider T, Belov K, Rens W, Waters PD, Pharo EA, Shaw G, Wong ES, Lefèvre CM, Nicholas KR, Kuroki Y, Wakefield MJ, Zenger KR, Wang C, Ferguson-Smith M, Nicholas FW, Hickford D, Yu H, Short KR, Siddle HV, Frankenberg SR, Chew KY, Menzies BR, Stringer JM, Suzuki S, Hore TA, Delbridge ML, et al.: Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development. Genome Biol 2011, 12(8):R81. BioMed Central Full Text
• [38]Murtagh VJ, O’Meally D, Sankovic N, Delbridge ML, Kuroki Y, Boore JL, Toyoda A, Jordan KS, Pask AJ, Renfree MB, Fujiyama A, Graves JA, Waters PD: Evolutionary history of novel genes on the tammar wallaby Y chromosome: Implications for sex chromosome evolution. Genome Res 2012, 22(3):498-507.
• [39]Al Nadaf S, Waters PD, Koina E, Deakin JE, Jordan KS, Graves JA: Activity map of the tammar X chromosome shows that marsupial X inactivation is incomplete and escape is stochastic. Genome Biol 2010, 11(12):R122. BioMed Central Full Text
• [40]Deakin JE, Koina E, Waters PD, Doherty R, Patel VS, Delbridge ML, Dobson B, Fong J, Hu Y, van den Hurk C, Pask AJ, Shaw G, Smith C, Thompson K, Wakefield MJ, Yu H, Renfree MB, Graves JA: Physical map of two tammar wallaby chromosomes: a strategy for mapping in non-model mammals. Chromosome Res 2008, 16(8):1159-1175.
• [41]Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, Mangan M, Nekrutenko A, Taylor J: Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol 2010, 0 19:Unit-19.1021.
• [42]Langmead B, Trapnell C, Pop M, Salzberg SL: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10(3):R25. BioMed Central Full Text
• [43]Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R: The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25(16):2078-2079.
• [44]Thorvaldsdottir H, Robinson JT, Mesirov JP: Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 2013, 14(2):178-192.
• [45]Koboldt DC, Chen K, Wylie T, Larson DE, McLellan MD, Mardis ER, Weinstock GM, Wilson RK, Ding L: VarScan: variant detection in massively parallel sequencing of individual and pooled samples. Bioinformatics 2009, 25(17):2283-2285.
• [46]Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG: Primer3–new capabilities and interfaces. Nucleic Acids Res 2012, 40(15):e115.