Conservation of regional variation in sex-specific sex chromosome regulation

Genetics

Volumn 201, Issue 2, 2015, Pages 587-598

  Wright, Alison E ^a   Zimmer, Fabian ^a   Harrison, Peter W ^a   Mank, Judith E ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Male hypermethylated region; Sex biased gene expression

Indexed keywords

ADULT; ANAS PLATYRHYNCHOS; ANIMAL TISSUE; ANSER CYGNOIDES; ARTICLE; AUTOSOME; DNA METHYLATION; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; GENETIC VARIABILITY; HEMIZYGOSITY; MALE; MELEAGRIS GALLOPAVO; MOLECULAR PHYLOGENY; NONHUMAN; NUMIDA MELEAGRIS; OVARY FOLLICLE DEVELOPMENT; PAVO CRISTATUS; PHASIANUS COLCHICUS; PRIORITY JOURNAL; PURIFYING SELECTION; SAMPLING BIAS; SEX CHROMOSOME; SEX DIFFERENCE; ANIMAL; CHICKEN; GENETICS; MOLECULAR EVOLUTION;

ANIMALS; CHICKENS; DNA METHYLATION; DOSAGE COMPENSATION, GENETIC; EVOLUTION, MOLECULAR; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; SEX CHROMOSOMES;

EID: 84943650369     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.115.179234     Document Type: Article

References (60)

1. Alfoeldi, J., F. Di Palma, M. Grabherr, C. Williams, L. Kong et al., 2011 The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477: 587-591.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman, 1990 Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
3. Axelsson, E., L. Hultin-Rosenberg, M. Brandström, M. Zwahlen, D. F. Clayton et al., 2008 Natural selection in avian protein-coding genes expressed in brain. Mol. Ecol. 17: 3008-3017.
4. Bachtrog, D., 2013 Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat. Rev. Genet. 14: 113-124.
5. Barber, D. L., E. J. Sanders, R. Aebersold, and W. J. Schneider, 1991 The receptor for yolk lipoprotein deposition in the chicken oocyte. J. Biol. Chem. 266: 18761-18770.
6. Benjamini, Y., and Y. Hochberg, 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57: 289-300.
7. Bisoni, L., L. Batlle-Morera, A. Bird, M. Suzuki, and H. Mcqueen, 2005 Female-specific hyperacetylation of histone H4 in the chicken Z chromosome. Chromosome Res. 13: 205-214.
8. Caetano, L. C., F. G. O. Gennaro, K. Coelho, F. M. Araujo, R. A. Vila et al., 2014 Differential expression of the MHM region and of sex-determining-related genes during gonadal development in chicken embryos. Genet. Mol. Res. 13: 838-849.
9. Carrel, L., and H. F. Willard, 2005 X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434: 400-404.
10. Charlesworth, B., J. A. Coyne, and N. H. Barton, 1987 The relative rates of evolution of sex chromosomes and autosomes. Am. Nat. 130: 113-146.
11. Dean, R., F. Zimmer, and J. E. Mank, 2015 Deficit of mito-nuclear genes on the human X chromosome predates sex chromosome formation. Genome Biol. Evol. 7: 636-641
12. Deng, X., and V. H. Meller, 2006 Non-coding RNA in fly dosage compensation. Trends Biochem. Sci. 31: 526-532.
13. Eden, E., D. Lipson, S. Yogev, and Z. Yakhini, 2007 Discovering motifs in ranked lists of DNA sequences. PLoS Comput. Biol. 3: e39.
14. Eden, E., R. Navon, I. Steinfeld, D. Lipson, and Z. Yakhini, 2009 GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10: 48.
15. Ellegren, H., L. Hultin-Rosenberg, B. Brunstrom, L. Dencker, K. Kultima et al., 2007 Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes. BMC Biol. 5: 40.
16. Flicek, P., I. Ahmed, M. R. Amode, D. Barrell, K. Beal et al., 2013 Ensembl 2013. Nucleic Acids Res. 41: D48-55.
17. Grabherr, M. G., B. J. Haas, M. Yassour, J. Z. Levin, D. A. Thompson et al., 2011 Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29: 644-652.
18. Harrison, P. W., A. E. Wright, F. Zimmer, R. Dean, S. H. Montgomery et al., 2015 Sexual selection drives evolution and rapid turnover of male gene expression. Proc. Natl. Acad. Sci. USA 112: 4393-4398.
19. Hu, S., H. Liu, Z. Pan, L. Xia, X. Dong et al., 2014 Molecular cloning, expression profile and transcriptional modulation of two splice variants of very low density lipoprotein receptor during ovarian follicle development in geese (Anser cygnoide). Anim. Reprod. Sci. 149: 281-296.
20. Itoh, Y., K. Kampf, and A. P. Arnold, 2011 Possible differences in the two Z chromosomes in male chickens and evolution of MHM sequences in Galliformes. Chromosoma 120: 587-598.
21. Itoh, Y., E. Melamed, X. Yang, K. Kampf, S. Wang et al., 2007 Dosage compensation is less effective in birds than in mammals. J. Biol. 6: 2.
22. Itoh, Y., K. Replogle, Y. H. Kim, J. Wade, D. F. Clayton et al., 2010 Sex bias and dosage compensation in the zebra finch vs. chicken genomes: general and specialized patterns among birds. Genome Res. 20: 512-518.
23. Li, B., and C. N. Dewey, 2011 RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12: 323.
24. Lohse, M., A. M. Bolger, A. Nagel, A. R. Fernie, J. E. Lunn et al., 2012 RobiNA: A user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Res. 40: W622-627.
25. Loytynoja, A., and N. Goldman, 2005 An algorithm for progressive multiple alignment of sequences with insertions. Proc. Natl. Acad. Sci. USA 102: 10557-10562.
26. Mank, J. E., 2013 Sex chromosome dosage compensation: definitely not for everyone. Trends Genet. 29: 677-683.
27. Mank, J. E., and H. Ellegren, 2009 All dosage compensation is local: gene-by-gene regulation of sex-biased expression on the chicken Z chromosome. Heredity 102: 312-320.
28. Meisel, R. P., and T. Connallon, 2013 The faster-X effect: integrating theory and data. Trends Genet. 29: 537-544.
29. Melamed, E., and A. P. Arnold, 2007 Regional differences in dosage compensation on the chicken Z chromosome. Genome Biol. 8: R202.
30. Melamed, E., D. Elashoff, and A. P. Arnold, 2009 Evaluating dosage compensation on the chicken Z chromosome: should effective dosage compensation eliminate sexual bias. Heredity 103: 357-359.
31. Moghadam, H. K., P. W. Harrison, G. Zachar, T. Szekely, and J. E. Mank, 2013 The plover neurotranscriptome assembly: transcriptomic analysis in an ecological model species without a reference genome. Mol. Ecol. Resour. 13: 696-705.
32. Nätt, D., B. Agnvall, and P. Jensen, 2014 Large sex differences in chicken behavior and brain gene expression coincide with few differences in promoter DNA-methylation. PLoS One 9: e96376.
33. Naurin, S., B. Hansson, D. Hasselquist, Y.-H. Kim, and S. Bensch, 2011 The sex-biased brain: sexual dimorphism in gene expression in two species of songbirds. BMC Genomics 12: 37.
34. Ohno, S., 1967 Sex Chromosomes and Sex Linked Genes. Springer, Berlin.
35. R Core Team, 2014 R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. Available at: http://www.R-project.org/.
36. Rens, W., M. S. Wallduck, F. L. Lovell, M. A. Ferguson-Smith, and A. C. Ferguson-Smith, 2010 Epigenetic modifications on X chromosomes in marsupial and monotreme mammals and implications for evolution of dosage compensation. Proc. Natl. Acad. Sci. USA 107: 17657-17662.
37. Rice, W. R., 1984 Sex chromosomes and the evolution of sexual dimorphism. Evolution 38: 735-742.
38. Robinson, M. D., D. J. Mccarthy, and G. K. Smyth, 2010 edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
39. Schultheiß, R., H. M. Viitaniemi, and E. H. Leder, 2015 Spatial dynamics of evolving dosage compensation in a young sex chromosome system. Genome Biol. Evol. 7: 581-590.
40. Skinner, B. M., L. B. W. Robertson, H. G. Tempest, E. J. Langley, D. Ioannou et al., 2009 Comparative genomics in chicken and Pekin duck using FISH mapping and microarray analysis. BMC Genomics 10: 357.
41. Smith, C. A., K. N. Roeszler, T. Ohnesorg, D. M. Cummins, P. G. Farlie et al., 2009 The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461: 267-271.
42. Stiglec, R., T. Ezaz, and J. M. Graves, 2007 A new look at the evolution of avian sex chromosomes. Cytogenet. Genome Res. 117: 103-109.
43. Teranishi, M., Y. Shimada, T. Hori, O. Nakabayashi, T. Kikuchi et al., 2001 Transcripts of the MHM region on the chicken Z chromosome accumulate as non-coding RNA in the nucleus of female cells adjacent to the DMRT1 locus. Chromosome Res. 9: 147-165.
44. Toups, M. A., J. B. Pease, and M. W. Hahn, 2011 No excess gene movement is detected off the avian or lepidopteran Z chromosome. Genome Biol. Evol. 3: 1381-1390.
45. Uebbing, S., A. Kunstner, H. Makinen, and H. Ellegren, 2013 Transcriptome sequencing reveals the character of incomplete dosage compensation across multiple tissues in flycatchers. Genome Biol. Evol. 5: 1555-1566.
46. Van Tuinen, M., and S. B. Hedges, 2001 Calibration of avian molecular clocks. Mol. Biol. Evol. 18: 206-213.
47. Vicoso, B., and B. Charlesworth, 2009 Effective population size and the Faster-X effect: an extended model. Evolution 63: 2413-2426.
48. Vicoso, B., V. B. Kaiser, and D. Bachtrog, 2013 Sex-biased gene expression at homomorphic sex chromosomes in emus and its implication for sex chromosome evolution. Proc. Natl. Acad. Sci. USA 110: 6453-6458.
49. Wang, X.-J., Y. Li, Q.-Q. Song, Y.-Y. Guo, H.-C. Jiao et al., 2013 Corticosterone regulation of ovarian follicular development is dependent on the energy status of laying hens. J. Lipid Res. 54: 1860-1876.
50. Wang, Y., H. Tang, J. D. Debarry, X. Tan, J. Li et al., 2012 MC ScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40: e49.
51. Wang, Z., J. Zhang, W. Yang, N. An, P. Zhang et al., 2014 Temporal genomic evolution of bird sex chromosomes. BMC Evol. Biol. 14: 250.
52. Wolf, J. B. W., and J. Bryk, 2011 General lack of global dosage compensation in ZZ/ZW systems? Broadening the perspective with RNA-seq. BMC Genomics 12: 91.
53. Wright, A. E., P. W. Harrison, S. H. Montgomery, M. A. Pointer, and J. E. Mank, 2014 Independent stratum formation on the avian sex chromosomes reveals inter-chromosomal gene conversion and predominance of purifying selection on the W chromosomes. Evolution 68: 3281-3295.
54. Wright, A. E., P. W. Harrison, F. Zimmer, S. H. Montgomery, M. A. Pointer et al., 2015 Variation in promiscuity and sexual selection drives avian rate of Faster-Z evolution. Mol. Ecol. 24: 1218-1235.
55. Wright, A. E., H. K. Moghadam, and J. E. Mank, 2012 Trade-off between selection for dosage compensation and masculinization on the avian Z chromosome. Genetics 192: 1433-1445.
56. Yang, F., T. Babak, J. Shendure, and C. M. Disteche, 2010a Global survey of escape from X inactivation by RNA-sequencing in mouse. Genome Res. 20: 614-622.
57. Yang, X., J. Zheng, G. Xu, L. Qu, S. Chen et al., 2010b Exogenous cMHM regulates the expression of DMRT1 and ERa in avian testes. Mol. Biol. Rep. 37: 1841-1847.
58. Yang, Z., 2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24: 1586-1591.
59. Zhang, R., L. Hao, L. Wang, M. Chen, W. Li et al., 2013 Gene expression analysis of induced pluripotent stem cells from aneuploid chromosomal syndromes. BMC Genomics 14(Suppl. 5): S8.
60. Zhou, Q., J. Zhang, D. Bachtrog, N. An, Q. Huang et al., 2014 Complex evolutionary trajectories of sex chromosomes across bird taxa. Science 346:1246338.