The evolution of X chromosome inactivation in mammals: The demise of Ohno's hypothesis?

Cellular and Molecular Life Sciences

Volumn 71, Issue 8, 2014, Pages 1383-1394

  Pessia, Eugénie ^a   Engelstädter, Jan ^b   Marais, Gabriel A B ^a,c  

^a UNIVERSITÉ LYON 1   (France)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

Dosage compensation; Dosage sensitive genes; Parental antagonism model; RNAseq data; Sex chromosomes; Sex determination

Indexed keywords

AUTOSOME; GENE DOSAGE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HUMAN; MAMMAL; MOLECULAR EVOLUTION; NONHUMAN; REVIEW; X CHROMOSOME INACTIVATION;

MAMMALIA;

ANIMALS; BIOLOGICAL EVOLUTION; GENES, X-LINKED; MAMMALS; MODELS, GENETIC; PHYLOGENY; X CHROMOSOME INACTIVATION;

EID: 84897110549     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1499-6     Document Type: Review

References (75)

1. Veyrunes F, Waters PD, Miethke P, Rens W, McMillan D, Alsop AE, Grutzner F, Deakin JE, Whittington CM, Schatzkamer K, Kremitzki CL, Graves T, Ferguson-Smith MA, Warren W, Marshall Graves JA (2008) Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Res 18(6):965-973. doi:10.1101/gr.7101908 (Pubitemid 351793069)
2. Potrzebowski L, Vinckenbosch N, Marques AC, Chalmel F, Jegou B, Kaessmann H (2008) Chromosomal gene movements reflect the recent origin and biology of therian sex chromosomes. PLoS Biol 6(4):e80. doi:10.1371/journal.pbio.0060080
3. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, Repping S, Pyntikova T, Ali J, Bieri T, Chinwalla A, Delehaunty A, Delehaunty K, Du H, Fewell G, Fulton L, Fulton R, Graves T, Hou S-F, Latrielle P, Leonard S, Mardis E, Maupin R, McPherson J, Miner T, Nash W, Nguyen C, Ozersky P, Pepin K, Rock S, Rohlfing T, Scott K, Schultz B, Strong C, Tin-Wollam A, Yang S-P, Waterston RH, Wilson RK, Rozen S, Page DC (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:825-837 (Pubitemid 36781267)
4. Ohno S, Kaplan WD, Kinosita R (1959) Formation of the sex chromatin by a single X-chromosome in liver cells of Rattus norvegicus. Exp Cell Res 18(2):415-419
5. Lyon MF (1961) Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190:372-373
6. Ohno S (1967) Sex chromosomes and sex linked genes. Springer, Berlin Heidelberg New York
7. Deakin JE, Chaumeil J, Hore TA, Marshall Graves JA (2009) Unravelling the evolutionary origins of X chromosome inactivation in mammals: insights from marsupials and monotremes. Chromosome Res 17(5):671-685. doi:10.1007/s10577-009- 9058-6
8. Lee JT (2011) Gracefully ageing at 50, X-chromosome inactivation becomes a paradigm for RNA and chromatin control. Nat Rev Mol Cell Biol 12(12):815-826. doi:10.1038/nrm3231
9. Livernois AM, Graves JA, Waters PD (2012) The origin and evolution of vertebrate sex chromosomes and dosage compensation. Heredity (Edinb) 108(1):50-58. doi:10.1038/hdy.2011.106
10. Jeon Y, Sarma K, Lee JT (2012) New and Xisting regulatory mechanisms of X chromosome inactivation. Curr Opin Genet Dev 22(2):62-71. doi:10.1016/j.gde. 2012.02.007
11. Disteche CM (2012) Dosage compensation of the sex chromosomes. Annu Rev Genet 46:537-560. doi:10.1146/annurev-genet-110711-155454
12. Gribnau J, Grootegoed JA (2012) Origin and evolution of X chromosome inactivation. Curr Opin Cell Biol 24(3):397-404. doi:10.1016/j.ceb.2012.02.004
13. Dupont C, Gribnau J (2013) Different flavors of X-chromosome inactivation in mammals. Curr Opin Cell Biol 25(3):314-321. doi:10.1016/j.ceb.2013.03.001
14. Ohhata T, Wutz A (2013) Reactivation of the inactive X chromosome in development and reprogramming. Cell Mol Life Sci 70(14):2443-2461. doi:10.1007/s00018-012-1174-3
15. Schulz EG, Heard E (2013) Role and control of X chromosome dosage in mammalian development. Curr Opin Genet Dev 23(2):109-115. doi:10.1016/j.gde. 2013.01.008
16. Gontan C, Achame EM, Demmers J, Barakat TS, Rentmeester E, van Ijcken W, Grootegoed JA, Gribnau J (2012) RNF12 initiates X-chromosome inactivation by targeting REX1 for degradation. Nature 485(7398):386-390. doi:10.1038/ nature11070
17. Engreitz JM, Pandya-Jones A, McDonel P, Shishkin A, Sirokman K, Surka C, Kadri S, Xing J, Goren A, Lander ES, Plath K, Guttman M (2013) The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science 341(6147):1237973. doi:10.1126/science.1237973
18. Chow JC, Ciaudo C, Fazzari MJ, Mise N, Servant N, Glass JL, Attreed M, Avner P, Wutz A, Barillot E, Greally JM, Voinnet O, Heard E (2010) LINE-1 activity in facultative heterochromatin formation during X chromosome inactivation. Cell 141(6):956-969. doi:10.1016/j.cell.2010.04.042
19. Carrel L, Willard HF (2005) X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434:400-404 (Pubitemid 40469185)
20. Zhang Y, Morales AC, Jiang M, Zhu Y, Hu L, Urrutia AO, Kong X, Hurst LD (2013) Genes that escape X-inactivation in humans have high intraspecific variability in expression, are associated with mental impairment but are not slow evolving. Mol Biol Evol. doi:10.1093/molbev/mst148
21. Duret L, Chureau C, Samain S, Weissenbach J, Avner P (2006) The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 312:1653-1655 (Pubitemid 43902664)
22. Nguyen DK, Disteche CM (2006) Dosage compensation of the active X chromosome in mammals. Nat Genet 38(1):47-53
23. Gupta V, Parisi M, Sturgill D, Nuttall R, Doctolero M, Dudko OK, Malley JD, Eastman PS, Oliver B (2006) Global analysis of X-chromosome dosage compensation. J. Biol 5(1):3. doi:10.1186/jbiol30
24. Talebizadeh Z, Simon SD, Butler MG (2006) X chromosome gene expression in human tissues: male and female comparisons. Genomics 88(6):675-681. doi:10.1016/j.ygeno.2006.07.016 (Pubitemid 44739205)
25. Lin H, Gupta V, Vermilyea MD, Falciani F, Lee JT, O'Neill LP, Turner BM (2007) Dosage compensation in the mouse balances up-regulation and silencing of X-linked genes. PLoS Biol 5(12):e326. doi:10.1371/journal.pbio.0050326
26. Johnston CM, Lovell FL, Leongamornlert DA, Stranger BE, Dermitzakis ET, Ross MT (2008) Large-scale population study of human cell lines indicates that dosage compensation is virtually complete. PLoS Genet 4(1):e9. doi:10.1371/journal.pgen.0040009
27. Xiong Y, Chen X, Chen Z, Wang X, Shi S, Zhang J, He X (2010) RNA sequencing shows no dosage compensation of the active X-chromosome. Nat Genet 42(12):1043-1047
28. Deng X, Hiatt JB, Nguyen DK, Ercan S, Sturgill D, Hillier LW, Schlesinger F, Davis CA, Reinke VJ, Gingeras TR, Shendure J, Waterston RH, Oliver B, Lieb JD, Disteche CM (2011) Evidence for compensatory upregulation of expressed X-linked genes in mammals, Caenorhabditis elegans and Drosophila melanogaster. Nat Genet 43(12):1179-1185. doi:10.1038/ng.948
29. He X, Chen X, Xiong Y, Chen Z, Wang X, Shi S, Wang X, Zhang J (2011) He et al. reply. Nat Genet 43(12):1171-1172
30. Kharchenko PV, Xi R, Park PJ (2011) Evidence for dosage compensation between the X chromosome and autosomes in mammals. Nat Genet 43(12):1167-1169. doi:10.1038/ng.991 (author reply 1171-1162)
31. Lin H, Halsall JA, Antczak P, O'Neill LP, Falciani F, Turner BM (2011) Relative overexpression of X-linked genes in mouse embryonic stem cells is consistent with Ohno's hypothesis. Nat Genet 43(12):1169-1170. doi:10.1038/ng.992 (author reply 1171-1162)
32. Pessia E, Makino T, Bailly-Bechet M, McLysaght A, Marais GA (2012) Mammalian X chromosome inactivation evolved as a dosage-compensation mechanism for dosage-sensitive genes on the X chromosome. Proc Natl Acad Sci USA 109(14):5346-5351. doi:10.1073/pnas.1116763109
33. Julien P, Brawand D, Soumillon M, Necsulea A, Liechti A, Schutz F, Daish T, Grutzner F, Kaessmann H (2012) Mechanisms and evolutionary patterns of mammalian and avian dosage compensation. PLoS Biol 10(5):e1001328. doi:10.1371/journal.pbio.1001328
34. Lin F, Xing K, Zhang J, He X (2012) Expression reduction in mammalian X chromosome evolution refutes Ohno's hypothesis of dosage compensation. Proc Natl Acad Sci USA 109(29):11752-11757. doi:10.1073/pnas.1201816109
35. Yildirim E, Sadreyev RI, Pinter SF, Lee JT (2011) X-chromosome hyperactivation in mammals via nonlinear relationships between chromatin states and transcription. Nat Struct Mol Biol 19(1):56-61. doi:10.1038/nsmb.2195
36. Adler DA, Rugarli EI, Lingenfelter PA, Tsuchiya K, Poslinski D, Liggitt HD, Chapman VM, Elliott RW, Ballabio A, Disteche CM (1997) Evidence of evolutionary up-regulation of the single active X chromosome in mammals based on Clc4 expression levels in Mus spretus and Mus musculus. Proc Natl Acad Sci USA 94(17):9244-9248 (Pubitemid 27357814)
37. Brawand D, Soumillon M, Necsulea A, Julien P, Csardi G, Harrigan P, Weier M, Liechti A, Aximu-Petri A, Kircher M, Albert FW, Zeller U, Khaitovich P, Grutzner F, Bergmann S, Nielsen R, Paabo S, Kaessmann H (2011) The evolution of gene expression levels in mammalian organs. Nature 478(7369):343-348. doi:10.1038/nature10532
38. Zhang YE, Vibranovski MD, Landback P, Marais GA, Long M (2010) Chromosomal redistribution of male-biased genes in mammalian evolution with two bursts of gene gain on the X chromosome. PLoS Biol 8(10). doi:10.1371/journal. pbio.1000494
39. Malone JH, Cho DY, Mattiuzzo NR, Artieri CG, Jiang L, Dale RK, Smith HE, McDaniel J, Munro S, Salit M, Andrews J, Przytycka TM, Oliver B (2012) Mediation of Drosophila autosomal dosage effects and compensation by network interactions. Genome Biol 13(4):r28. doi:10.1186/gb-2012-13-4-r28
40. Birchler JA (2012) Claims and counterclaims of X-chromosome compensation. Nat Struct Mol Biol 19(1):3-5. doi:10.1038/nsmb.2218
41. Papp B, Pal C, Hurst LD (2003) Dosage sensitivity and the evolution of gene families in yeast. Nature 424(6945):194-197. doi:10.1038/nature01771 (Pubitemid 36858686)
42. Hall DW, Wayne ML (2013) Ohno's "peril of hemizygosity" revisited: gene loss, dosage compensation, and mutation. Genome Biol Evol 5(1):1-15. doi:10.1093/gbe/evs106
43. Mank JE, Hosken DJ, Wedell N (2011) Some inconvenient truths about sex chromosome dosage compensation and the potential role of sexual conflict. Evolution 65(8):2133-2144. doi:10.1111/j.1558-5646.2011.01316.x
44. Wright AE, Mank JE (2012) Battle of the sexes: conflict over dosage-sensitive genes and the origin of X chromosome inactivation. Proc Natl Acad Sci USA 109(14):5144-5145. doi:10.1073/pnas.1202905109
45. Veitia RA (2005) Gene dosage balance: deletions, duplications and dominance. Trends Genet 21(1):33-35. doi:10.1016/j.tig.2004.11.002
46. Deutschbauer AM, Jaramillo DF, Proctor M, Kumm J, Hillenmeyer ME, Davis RW, Nislow C, Giaever G (2005) Mechanisms of haploinsufficiency revealed by genome-wide profiling in yeast. Genetics 169:1915-1925 (Pubitemid 40695608)
47. Gout J, Kahn D, Duret L (2010) The relationship among gene expression, the evolution of gene dosage, and the rate of protein evolution. PLoS Genet 6(5):e1000944. doi:10.1371/journal.pgen.1000944
48. Engelstadter J, Haig D (2008) Sexual antagonism and the evolution of X chromosome inactivation. Evolution 62(8):2097-2104. doi:10.1111/j.1558-5646. 2008.00431.x (Pubitemid 352033266)
49. Haig D (2000) The kinship theory of genomic imprinting. Annu Rev Ecol Syst 31:9-32
50. Haig D (2006) Self-imposed silence: parental antagonism and the evolution of X-chromosome inactivation. Evolution 60(3):440-447
51. Haig D (2006) Intragenomic politics. Cytogenet Genome Res 113(1-4):68-74. doi:10.1159/000090816
52. Necsulea A, Soumillon M, Liechti A, Daish T, Baker JC, Grützner F, Kaessmann H (2013) Functionality and evolution of lncRNA repertoires and expression patterns in tetrapods. Nature (in press)
53. Livernois AM, Waters SA, Deakin JE, Marshall Graves JA, Waters PD (2013) Independent evolution of transcriptional inactivation on sex chromosomes in birds and mammals. PLoS Genet 9(7):e1003635. doi:10.1371/journal.pgen.1003635
54. Collignon J, Sockanathan S, Hacker A, Cohen-Tannoudji M, Norris D, Rastan S, Stevanovic M, Goodfellow PN, Lovell-Badge R (1996) A comparison of the properties of Sox-3 with Sry and two related genes, Sox-1 and Sox-2. Development 122(2):509-520 (Pubitemid 26054140)
55. Splinter E, de Wit E, Nora EP, Klous P, van de Werken HJ, Zhu Y, Kaaij LJ, van Ijcken W, Gribnau J, Heard E, de Laat W (2011) The inactive X chromosome adopts a unique three-dimensional conformation that is dependent on Xist RNA. Genes Dev 25(13):1371-1383. doi:10.1101/gad.633311
56. Charlesworth B, Charlesworth D (1978) A model for the evolution of dioecy and gynodioecy. Amer Nat 112:975-997
57. Bachtrog D (2013) Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 14(2):113-124. doi:10.1038/nrg3366
58. Rice WR (1987) The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex-chromosomes. Evolution 41:911-914
59. Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95(2):118-128 (Pubitemid 41133194)
60. 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 (2012) Rsx is a metatherian RNA with Xist-like properties in X-chromosome inactivation. Nature 487(7406):254-258. doi:10.1038/nature11171
61. Wang X, Douglas KC, Vandeberg JL, Clark A, Samollow PB (2013) Chromosome-wide profiling of X-chromosome inactivation and epigenetic states in fetal brain and placenta of the opossum, Monodelphis domestica. Genome Res. doi:10.1101/gr.161919.113
62. Okamoto I, Patrat C, Thepot D, Peynot N, Fauque P, Daniel N, Diabangouaya P, Wolf JP, Renard JP, Duranthon V, Heard E (2011) Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development. Nature 472(7343):370-374. doi:10.1038/nature09872
63. Tachibana M, Ma H, Sparman ML, Lee HS, Ramsey CM, Woodward JS, Sritanaudomchai H, Masterson KR, Wolff E, Jia Y, Mitalipov SM (2012) X-chromosome inactivation in monkey embryos and pluripotent stem cells. Dev Biol 371(2):146-155. doi:10.1016/j.ydbio.2012.08.009
64. Wang X, Miller DC, Clark AG, Antczak DF (2012) Random X inactivation in the mule and horse placenta. Genome Res 22(10):1855-1863. doi:10.1101/gr.138487. 112
65. Wang X, Soloway PD, Clark AG (2010) Paternally biased X inactivation in mouse neonatal brain. Genome Biol 11(7):R79. doi:10.1186/gb-2010-11-7-r79
66. Connallon T, Clark AG (2013) Sex-differential selection and the evolution of X inactivation strategies. PLoS Genet 9(4):e1003440. doi:10.1371/journal. pgen.1003440
67. Veyrunes F, Chevret P, Catalan J, Castiglia R, Watson J, Dobigny G, Robinson TJ, Britton-Davidian J (2010) A novel sex determination system in a close relative of the house mouse. Proc Biol Sci 277(1684):1049-1056. doi:10.1098/rspb 2009.1925
68. Castagne R, Rotival M, Zeller T, Wild PS, Truong V, Tregouet DA, Munzel T, Ziegler A, Cambien F, Blankenberg S, Tiret L (2011) The choice of the filtering method in microarrays affects the inference regarding dosage compensation of the active X-chromosome. PLoS ONE 6(9):e23956. doi:10.1371/journal.pone.0023956
69. Jue NK, Murphy MB, Kasowitz SD, Qureshi SM, Obergfell CJ, Elsisi S, Foley RJ, O'Neill RJ, O'Neill MJ (2013) Determination of dosage compensation of the mammalian X chromosome by RNA-seq is dependent on analytical approach. BMC Genomics 14(1):150. doi:10.1186/1471-2164-14-150
70. Mank JE, Ellegren H (2009) Sex bias in gene expression is not the same as dosage compensation. Heredity 103(5):434
71. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871-1971. Aldine-Atherton, Chicago, pp 136-179
72. Haig D (2002) Genomic imprinting and kinship. Rutgers University Press, New Brunswick
73. Charlesworth B, Charlesworth D (2000) The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci 355(1403):1563-1572
74. Charlesworth B (1978) Model for evolution of Y chromosomes and dosage compensation. Proc Natl Acad Sci USA 75(11):5618-5622
75. Charlesworth B (1996) The evolution of chromosomal sex determination and dosage compensation. Curr Biol 6(2):149-162