Spatial dynamics of evolving dosage compensation in a young sex chromosome system

Genome Biology and Evolution

Volumn 7, Issue 2, 2015, Pages 581-590

  Schultheiß, Roland ^a   Viitaniemi, Heidi M ^a   Leder, Erica H ^a  

^a UNIVERSITY OF TURKU   (Finland)

Author keywords

dosage compensation; gene expression; RNA sequencing; sex chromosome evolution; threespine stickleback; Y chromosome degeneration

Indexed keywords

GASTEROSTEUS;

TRANSCRIPTOME;

ANIMAL; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; MALE; MOLECULAR EVOLUTION; SEX CHROMOSOME; SEXUAL DEVELOPMENT; SMEGMAMORPHA;

ANIMALS; DOSAGE COMPENSATION, GENETIC; EVOLUTION, MOLECULAR; FEMALE; GENE EXPRESSION PROFILING; MALE; SEX CHARACTERISTICS; SEX CHROMOSOMES; SMEGMAMORPHA; TRANSCRIPTOME;

EID: 84928262851     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evv013     Document Type: Article

References (49)

1. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol. 11:R106.
2. Bachtrog D. 2013. Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet. 14:113-124.
3. Bachtrog D, et al. 2011. Are all sex chromosomes created equal? Trends Genet. 27:350-357.
4. Bell, MA. 1994. Paleobiology and evolution of threespine stickleback. In: Bell, MA and Foster, SA, editors. The Evolutionary Biology of the Threespine Stickleback. Oxford: Oxford University Press. p. 439-471.
5. Bell MA, Stewart JD, Park PJ. 2009. The world's oldest fossil threespine stickleback fish. Copeia 2009:256-265.
6. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc. 57:289-300.
7. Canty A, Ripley BD. 2014. boot: Bootstrap R (S-Plus) Functions. Available at: http://cran.r-project.org/web/packages/boot/.
8. Carrel L, Willard HF. 2005. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434:400-404.
9. Charlesworth B. 1996. The evolution of chromosomal sex determination and dosage compensation. Curr Biol. 6:149-162.
10. Charlesworth D, Charlesworth B,Marais G. 2005. Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118-128.
11. Chibalina MV, Filatov DA. 2011. Plant Y chromosome degeneration is retarded by haploid purifying selection. Curr Biol. 21:1475-1479.
12. Cortez D, et al. 2014. Origins and functional evolution of Y chromosomes across mammals. Nature 508:488-493.
13. Ellegren H, et al. 2007. Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes. BMC Biol. 5:40.
14. Ercan S, et al. 2007. X chromosome repression by localization of the C. elegans dosage compensation machinery to sites of transcription initiation. Nat Genet. 39:403-408.
15. Gelbart ME, Kuroda MI. 2009. Drosophila dosage compensation: a complex voyage to the X chromosome. Development 136: 1399-1410.
16. Hall DW, Wayne ML. 2013. Ohno's 'peril of hemizygosity' revisited: gene loss, dosage compensation, and mutation. Genome Biol Evol. 5:1-15.
17. Harrison PW, Mank J, Wedell N. 2012. Incomplete sex chromosome dosage compensation in the Indian meal moth, Plodia interpunctella, based on de novo transcriptome assembly. Genome Biol Evol. 4: 1118-1126.
18. Itoh Y, et al. 2007. Dosage compensation is less effective in birds than in mammals. J Biol. 6:2.
19. Julien P, et al. 2012. Mechanisms and evolutionary patterns ofmammalian and avian dosage compensation. PLoS Biol. 10:e1001328.
20. Kaiser VB, Zhou Q, Bachtrog D. 2011. Nonrandom gene loss from the Drosophila miranda neo-Y chromosome. Genome Biol Evol. 3: 1329-1337.
21. Leder EH, et al. 2010. Female-biased expression on the X chromosome as a key step in sex chromosome evolution in threespine sticklebacks. Mol Biol Evol. 27:1495-1503.
22. Li H, et al. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078-2079.
23. Mank J. 2009. Sex chromosomes and the evolution of sexual dimorphism: lessons from the genome. Am Nat. 173:141-150.
24. Mank J. 2013. Sex chromosome dosage compensation: definitely not for everyone. Trends Genet. 29:677-683.
25. Mank J, Ellegren H. 2009. All dosage compensation is local: Gene-by-gene regulation of sex-biased expression on the chicken Z chromosome. Heredity 102:312-320.
26. Muyle A, et al. 2012. Rapid de novo evolution of X chromosome dosage compensation in Silene latifolia, a plant with young sex chromosomes. PLoS Biol. 10:e1001308.
27. Ohno S. 1967. Sex chromosomes and sex-linked genes. Berlin (Germany): Springer.
28. Oliver B. 2007. Sex, dose, and equality. PLoS Biol. 5:e340.
29. Parsch J, Ellegren H. 2013. The evolutionary causes and consequences of sex-biased gene expression. Nat Rev Genet. 14:83-87.
30. Peichel CL, et al. 2004. The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome. Curr Biol. 14:1416-1424.
31. Pessia E, Makino T, Bailly-Bechet M, McLysaght A, Marais GAB. 2012. Mammalian X chromosome inactivation evolved as a dosagecompensation mechanism for dosage-sensitive genes on the X chromosome. Proc Natl Acad Sci U S A. 109:5346-5351.
32. Prince EG, Kirkland D, Demuth JP. 2010. Hyperexpression of the X chromosome in both sexes results in extensive female bias of X-linked genes in the flour beetle. Genome Biol Evol. 2:336-346.
33. R Core Team. 2013. R: a language and environment for statistical computing. Available at: http://www.R-project.org.
34. Rice WR. 1984. Sex chromosomes and the evolution of sexual dimorphism. Evolution 38:735-742.
35. Roesti M, Moser D, Berner D. 2013. Recombination in the threespine stickleback genome - patterns and consequences. Mol Ecol. 22: 3014-3027.
36. Ross JA, Peichel CL. 2008. Molecular cytogenetic evidence of rearrangements on the Y chromosome of the threespine stickleback fish. Genetics 179:2173-2182.
37. Ross JA, Urton JR, Boland J, Shapiro MD, Peichel CL. 2009. Turnover of sex chromosomes in the stickleback fishes (Gasterosteidae). PLoS Genet. 5:e1000391.
38. Sayres MAW,Makova KD. 2013. Gene survival and death on the human Y chromosome. Mol Biol Evol. 30:781-787.
39. Smeds L, Künstner A. 2011. ConDeTri - a content dependent read trimmer for llumina data. PLoS One 6:e26314.
40. Smith G, Chen Y-R, Blissard GW, Briscoe AD. 2014. Complete dosage compensation and sex-biased gene expression in the moth Manduca sexta. Genome Biol Evol. 6:526-537.
41. Trapnell C, et al. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 7: 562-578.
42. Uebbing S, Künstner A, Mäkinen H, Ellegren H. 2013. Transcriptome sequencing reveals the character of incomplete dosage compensation across multiple tissues in flycatchers. Genome Biol Evol. 5: 1555-1566.
43. Vicoso B, Bachtrog D. 2011. Lack of global dosage compensation in Schistosoma mansoni, a female-heterogametic parasite. Genome Biol Evol. 3:230-235.
44. Vicoso B, Charlesworth B. 2006. Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet. 7:645-653.
45. Vicoso B, Charlesworth B. 2009. The deficit of male-biased genes on the D. melanogaster X chromosome is expression-dependent: a consequence of dosage compensation? J Mol Evol. 68:576-583.
46. Wright AE,Moghadam HK, Mank J. 2012. Trade-off between selection for dosage compensation and masculinization on the avian Z chromosome. Genetics 192:1433-1445.
47. Yin T, Cook D, Lawrence M. 2012. ggbio: an R package for extending the grammar of graphics for genomic data. Genome Biol. 13:R77.
48. Zeileis A, Grothendieck G. 2005. zoo: S3 infrastructure for regular and irregular time series. J Stat Softw. 14:1-27.
49. Zhang YE, Vibranovski MD, Krinsky BH, Long M. 2010. Age-dependent chromosomal distribution of male-biased genes in Drosophila. Genome Res. 20:1526-1533.