Genomes of Ellobius species provide insight into the evolutionary dynamics of mammalian sex chromosomes

Genome Research

Volumn 26, Issue 9, 2016, Pages 1202-1210

  Mulugeta, Eskeatnaf ^a,b   Wassenaar, Evelyne ^a   Sleddens Linkels, Esther ^a   Van Ijcken, Wilfred F J ^a   Heard, Edith ^b   Grootegoed, J Anton ^a   Just, Walter ^c   Gribnau, Joost ^a   Baarends, Willy M ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b INSTITUT CURIE   (France)

^c UNIVERSITY OF ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GENOMIC DNA;

ARTICLE; CHROMOSOME LOSS; ELLOBIUS LUTESCENS; ELLOBIUS TALPINUS; FEMALE; GENE FUNCTION; GENE IDENTIFICATION; GENETIC CONSERVATION; GENOME; GENOME ANALYSIS; MALE; MAMMAL; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; PHYLOGENY; PLACENTAL MAMMAL; PRIORITY JOURNAL; RNA SEQUENCE; SEX DETERMINATION; SRY GENE; VOLE; X CHROMOSOME; X CHROMOSOME INACTIVATION; Y CHROMOSOME; ANIMAL; ARVICOLINAE; CHROMOSOME; GENETICS; KARYOTYPING; SEX CHROMOSOME; SEX DETERMINATION PROCESS;

ANIMALS; ARVICOLINAE; CHROMOSOMES, MAMMALIAN; FEMALE; KARYOTYPING; MALE; MAMMALS; MICE; SEX CHROMOSOMES; SEX DETERMINATION PROCESSES; X CHROMOSOME; Y CHROMOSOME;

EID: 84985001724     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.201665.115     Document Type: Article

References (75)

1. Arakawa Y, Nishida-Umehara C, Matsuda Y, Sutou S, Suzuki H. 2002. Xchromosomal localization ofmammalian Y-linked genes in two XO species of the Ryukyu spiny rat. Cytogenet Genome Res 99: 303-309.
2. Bachtrog D. 2013. Y-chromosome evolution: Emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 14: 113-124.
3. Bagheri-Fam S, Sreenivasan R, Bernard P, Knower KC, Sekido R, Lovell-Badge R, JustW, Harley VR. 2012. Sox9 gene regulation and the loss of the XY/XX sex-determining mechanism in the mole vole Ellobius lutescens. Chromosome Res 20: 191-199.
4. Bellott DW, Hughes JF, Skaletsky H, Brown LG, Pyntikova T, Cho TJ, Koutseva N, Zaghlul S, Graves T, Rock S, et al. 2014. Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators. Nature 508: 494-499.
5. Blackmon H, Demuth JP. 2015. The fragile Y hypothesis: Y chromosome aneuploidy as a selective pressure in sex chromosome and meiotic mechanism evolution. Bioessays 37: 942-950.
6. Brockdorff N, Turner BM. 2015. Dosage compensation in mammals. Cold Spring Harb Perspect Biol 7: A019406.
7. Cattanach BM, Pollard CE, Hawker SG. 1971. Sex-reversed mice: XX and XO males. Cytogenetics 10: 318-337.
8. Charlesworth B, Charlesworth D. 2000. The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci 355: 1563-1572.
9. The Chimpanzee Sequencing and Analysis Consortium. 2005. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437: 69-87.
10. Comptour A, Moretti C, Serrentino ME, Auer J, Ialy-Radio C, Ward MA, Toure A, Vaiman D, Cocquet J. 2014. SSTY proteins co-localize with the post-meiotic sex chromatin and interact with regulators of its expression. FEBS J 281: 1571-1584.
11. Cortez D, Marin R, Toledo-Flores D, Froidevaux L, Liechti A, Waters PD, Grutzner F, Kaessmann H. 2014. Origins and functional evolution of Y chromosomes across mammals. Nature 508: 488-493.
12. Deng X, Hiatt JB, Nguyen DK, Ercan S, Sturgill D, Hillier LW, Schlesinger F, Davis CA, Reinke VJ, Gingeras TR, et al. 2011. Evidence for compensatory upregulation of expressed X-linked genes in mammals, Caenorhabditis elegans and Drosophila melanogaster. Nat Genet 43: 1179-1185.
13. Deng X, Berletch JB, Ma W, Nguyen DK, Hiatt JB, Noble WS, Shendure J, Disteche CM. 2013. Mammalian X upregulation is associated with enhanced transcription initiation, RNA half-life, and MOF-mediated H4K16 acetylation. Dev Cell 25: 55-68.
14. Federici F, Mulugeta E, Schoenmakers S, Wassenaar E, Hoogerbrugge JW, van der Heijden GW, van Cappellen WA, Slotman JA, van IJcken WFJ, Laven JSE, et al. 2015. Incomplete meiotic sex chromosome inactivation in the domestic dog. BMC Genomics 16: 291.
15. Fredga K, Lyapunova E. 1991. Fertile males with two X chromosomes in Ellobius tancrei. Hereditas 115: 86-97.
16. Fredga K, Gropp A, Winking H, Frank F. 1976. Fertile XX- And XY- Type females in the wood lemming Myopus schisticolor. Nature 261: 225-227.
17. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29: 644-652.
18. Gropp A, Winking H, Frank F, Noack G, Fredga K. 1976. Sex-chromosome aberrations in wood lemmings (Myopus schisticolor). Cytogenet Cell Genet 17: 343-358.
19. Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, Sakamoto T, Fernandino JI, Somoza GM, Yokota M, Strussmann CA. 2012. A Y-linked anti- Müllerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci 109: 2955-2959.
20. Herpin A, Schartl M. 2015. Plasticity of gene-regulatory networks controlling sex determination: of masters, slaves, usual suspects, newcomers, and usurpators. EMBO Rep 16: 1260-1274.
21. Hinch AG, Altemose N, Noor N, Donnelly P, Myers SR. 2014. Recombination in the human pseudoautosomal region PAR1. PLoS Genet 10: E1004503.
22. Hughes JF, Page DC. 2015. The biology and evolution of mammalian Y chromosomes. Annu Rev Genet 49: 507-527.
23. Hughes JF, Skaletsky H, Brown LG, Pyntikova T, Graves T, Fulton RS, Dugan S, Ding Y, Buhay CJ, Kremitzki C, et al. 2012. Strict evolutionary conservation followed rapid gene loss on human and rhesus Y chromosomes. Nature 483: 82-86.
24. Hughes JF, Skaletsky H, Koutseva N, Pyntikova T, Page DC. 2015. Sex chromosome- To- Autosome transposition events counter Y-chromosome gene loss in mammals. Genome Biol 16: 104.
25. Hurst LD, Ellegren H. 1998. Sex biases in the mutation rate. Trends Genet 14: 446-452.
26. 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: E1001328.
27. Just W, Rau W, Voge lW, Akhverdian M, Fredga K, Graves JA, Lyapunova E. 1995. Absence of Sry in species of the vole Ellobius. Nat Genet 11: 117-118.
28. Just W, Baumstark A, Suss A, Graphodatsky A, Rens W, Schafer N, Bakloushinskaya I, Hameister H, Vogel W. 2007. Ellobius lutescens: sex determination and sex chromosome. Sex Dev 1: 211-221.
29. Kolomiets OL, Matveevsky SN, Bakloushinskaya IY. 2010. Sexual dimorphism in prophase I of meiosis in the northern mole vole (Ellobius talpinus Pallas, 1770) with isomorphic (XX) chromosomes in males and females. Comp Cytogenet 4: 55-66.
30. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R. 1991. Male development of chromosomally female mice trangenic for Sry. Nature 351: 117-121.
31. Kuroiwa A, Ishiguchi Y, Yamada F, Shintaro A, Matsuda Y. 2010. The process of a Y-loss event in an XO/XO mammal, the Ryukyu spiny rat. Chromosoma 119: 519-526.
32. Lesch BJ, Dokshin GA, Young RA, McCarrey JR, Page DC. 2013. A set of genes critical to development is epigenetically poised in mouse germ cells from fetal stages through completion of meiosis. Proc Natl Acad Sci 110: 16061-16066.
33. Li H. 2011. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27: 2987-2993.
34. Li H, Durbin R. 2010. Fast and accurate long-read alignment with Burrows- Wheeler transform. Bioinformatics 26: 589-595.
35. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing Subgroup. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078-2079.
36. 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 109: 11752-11757.
37. -ΔΔCTmethod. Methods 25: 402-408.
38. Lovell-Badge R, Robertson E. 1990. XY female mice resulting from a heritable mutation in the primary testis-determining gene, Tdy. Development 109: 635-646.
39. Lu J, Wu CI. 2005. Weak selection revealed by the whole-genome comparison of the X chromosome and autosomes of human and chimpanzee. Proc Natl Acad Sci 102: 4063-4067.
40. Lue Y, Rao PN, Sinha Hikim AP, Im M, Salameh WA, Yen PH, Wang C, Swerdloff RS. 2001. XXY male mice: An experimental model for Klinefelter syndrome. Endocrinology 142: 1461-1470.
41. Luoh S-W, Bain PA, Polakiewicz RD, Goodheart ML, Gardner H, Jaenisch R, Page DC. 1997. Zfx mutation results in small animal size reduced germ cell number in male and female mice. Development 124: 2275-2284.
42. Lyapunova EA, Vorontsov NN, Zakarjan GG. 1975. Zygotic mortality in Ellobius lutescens (Rodentia: Microtinae). Experientia 31: 417-418.
43. Lyon MF. 1961. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190: 372-373.
44. Mank JE, Vicoso B, Berlin S, Charlesworth B. 2010. Effective population size and the Faster-X effect: Empirical results and their interpretation. Evolution 64: 663-674.
45. Meisel RP, Connallon T. 2013. The faster-X effect: integrating theory and data. Trends Genet 29: 537-544.
46. Mueller JL, Mahadevaiah SK, Park PJ, Warburton PE, Page DC, Turner JM. 2008. The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression. Nat Genet 40: 794-799.
47. Mulugeta Achame E, Baarends WM, Gribnau J, Grootegoed JA. 2010a. Evaluating the relationship between spermatogenic silencing of the X chromosome and evolution of the Y chromosome in chimpanzee and human. PLoS One 5: E15598.
48. Mulugeta Achame E, Wassenaar E, Hoogerbrugge JW, Sleddens-Linkels E, Ooms M, Sun ZW, van IJcken WF, Grootegoed JA, Baarends WM. 2010b. The ubiquitin-conjugating enzyme HR6B is required for maintenance of X chromosome silencing in mouse spermatocytes and spermatids. BMC Genomics 11: 367.
49. Namekawa SH, Park PJ, Zhang LF, Shima JE, McCarrey JR, Griswold MD, Lee JT. 2006. Postmeiotic sex chromatin in the male germline of mice. Curr Biol 16: 660-667.
50. Necsulea A, Kaessmann H. 2014. Evolutionary dynamics of coding and non-coding transcriptomes. Nat Rev Genet 15: 734-748.
51. Nguyen DK, Disteche CM. 2006. Dosage compensation of the activeX chromosome in mammals. Nat Genet 38: 47-53.
52. Ohno S. 1967. Sex chromosomes and sex-linked genes. Springer-Verlag, Berlin.
53. Peters AH, Plug AW, van Vugt MJ, de Boer P. 1997. A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res 5: 66-68.
54. Romanenko SA, Sitnikova NA, Serdukova NA, Perelman PL, Rubtsova NV, Bakloushinskaya IY, Lyapunova EA, Just W, Ferguson-Smith MA, Yang F, et al. 2007. Chromosomal evolution of Arvicolinae (Cricetidae, Rodentia). II. The genome homology of two mole voles (genus Ellobius), the field vole and golden hamster revealed by comparative chromosome painting. Chromosome Res 15: 891-897.
55. Ross MT, Grafham DV, Coffey AJ, Scherer S, McLay K, Muzny D, Platzer M, Howell GR, Burrows C, Bird CP, et al. 2005. The DNA sequence of the human X chromosome. Nature 434: 325-337.
56. Sato Y, Shinka T, Sakamoto K, Ewis AA, Nakahori Y. 2010. The male-determining gene SRY is a hybrid of DGCR8 and SOX3, and is regulated by the transcription factor CP2. Mol Cell Biochem 337: 267-275.
57. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, Birol I. 2009. ABySS: A parallel assembler for short read sequence data. Genome Res 19: 1117-1123.
58. Sin HS, Ichijima Y, Koh E, Namiki M, Namekawa SH. 2012. Human postmeiotic sex chromatin and its impact on sex chromosome evolution. Genome Res 22: 827-836.
59. Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, Repping S, Pyntikova T, Ali J, Bieri T, et al. 2003. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423: 825-837.
60. Soh YQ, Alfoldi J, Pyntikova T, Brown LG, Graves T, Minx PJ, Fulton RS, Kremitzki C, Koutseva N, Mueller JL, et al. 2014. Sequencing the mouse Y chromosome reveals convergent gene acquisition and amplification on both sex chromosomes. Cell 159: 800-813.
61. Soumillon M, Necsulea A, Weier M, Brawand D, Zhang X, Gu H, Barthes P, Kokkinaki M, Nef S, Gnirke A, et al. 2013. Cellular source and mechanisms of high transcriptome complexity in the mammalian testis. Cell Rep 3: 2179-2190.
62. Su X, Zhu G, Ding X, Lee SY, Dou Y, Zhu B, Wu W, Li H. 2014. Molecular basis underlying histone H3 lysine- Arginine methylation pattern readout by Spin/Ssty repeats of Spindlin1. Genes Dev 28: 622-636.
63. Turner JM. 2007. Meiotic sex chromosome inactivation. Development 134: 1823-1831.
64. Vernet N, Mahadevaiah SK, Ojarikre OA, Longepied G, Prosser HM, Bradley A, Mitchell MJ, Burgoyne PS. 2011. The y-encoded gene zfy2 acts to remove cells with unpaired chromosomes at the first meiotic metaphase in male mice. Curr Biol 21: 787-793.
65. Vernet N, Mahadevaiah SK, Yamauchi Y, Decarpentrie F, Mitchell MJ, Ward MA, Burgoyne PS. 2014a. Mouse Y-linked Zfy1 and Zfy2 are expressed during the male-specific interphase between meiosis I and meiosis II and promote the second meiotic division. PLoS Genet 10: E1004444.
66. Vernet N, Szot M, Mahadevaiah SK, Ellis PJ, Decarpentrie F, Ojarikre OA, Rattigan A, Taketo T, Burgoyne PS. 2014b. The expression of Y-linked Zfy2 in XY mouse oocytes leads to frequent meiosis 2 defects, a high incidence of subsequent early cleavage stage arrest and infertility. Development 141: 855-866.
67. Vorontsov NN, Lyapunova E, Borissov YUM, Dovgal VE. 1980. Sex chromosome variability in mammals. Genetica 52/53: 361-372.
68. Winking H, Gropp A, Fredga K. 1981. Sex determination and phenotype in wood lemmings with XXY and related karyotypic anomalies. Hum Genet 58: 98-104.
69. Wolfe KH, Sharp PM. 1993. Mammalian gene evolution: nucleotide sequence divergence between mouse and rat. J Mol Evol 37: 441-456.
70. Xu B, Yang Z. 2013. PAMLX: A graphical user interface for PAML. Mol Biol Evol 30: 2723-2724.
71. Yamauchi Y, Riel JM, Stoytcheva Z, Ward MA. 2014. Two Y genes can replace the entire Y chromosome for assisted reproduction in the mouse. Science 343: 69-72.
72. Yamauchi Y, Riel JM, Ruthig VA, Ortega EA, Mitchell MJ, Ward MA. 2016. Two genes substitute for the mouse Y chromosome for spermatogenesis and reproduction. Science 351: 514-516.
73. Yang Z. 1997. PAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556.
74. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
75. Zhang C, Wang J, Long M, Fan C. 2013. gKaKs: The pipeline for genome-level Ka/Ks calculation. Bioinformatics 29: 645-646.