The genomic distribution of sex-biased genes in Drosophila serrata: X chromosome demasculinization, feminization, and hyperexpression in both sexes

Genome Biology and Evolution

Volumn 5, Issue 10, 2013, Pages 1986-1994

  Allen, Scott L ^a   Bonduriansky, Russell ^b   Chenoweth, Stephen F ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Dosage compensation; Drosophila; Sex biased gene expression; X chromosome

Indexed keywords

ANIMAL; ARTICLE; DROSOPHILA; FEMALE; FEMINIZATION; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; MALE; SEX DETERMINATION PROCESS; SEX-BIASED GENE EXPRESSION; SEXUAL DEVELOPMENT; X CHROMOSOMAL INHERITANCE; X CHROMOSOME;

DOSAGE COMPENSATION; DROSOPHILA; SEX-BIASED GENE EXPRESSION; X CHROMOSOME;

ANIMALS; DOSAGE COMPENSATION, GENETIC; DROSOPHILA; FEMALE; FEMINIZATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, X-LINKED; GENOMICS; MALE; SEX CHARACTERISTICS; SEX DETERMINATION PROCESSES; X CHROMOSOME;

EID: 84892536849     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evt145     Document Type: Article

References (48)

1. Bachtrog D, Toda NR, Lockton S. 2010. Dosage compensation and demasculinization of X chromosomes in Drosophila. Curr Biol. 20: 1476-1481.
2. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J R Stat Soc B. 57: 289-300.
3. Betran E, Thornton K, Long M. 2002. Retroposed new genes out of the X in Drosophila. Genome Res. 12:1854-1859.
4. Bhavsar RB, Makley LN, Tsonis PA. 2010. The other lives of ribosomal proteins. Hum Genomics. 4:327-344.
5. Bhutkar A, et al. 2008. Chromosomal rearrangement inferred from comparisons of 12 Drosophila genomes. Genetics 179:1657-1680.
6. Birchler JA. 2012. Claims and counterclaims of X-chromosome compensation. Nat Struct Mol Biol. 19:3-5.
7. Bonduriansky R, Chenoweth SF. 2009. Intralocus sexual conflict. Trends Ecol Evol. 24:280-288.
8. Carvalho BS, Irizarry RA. 2010. A framework for oligonucleotide microarray preprocessing. Bioinformatics 26:2363-2367.
9. Connallon T, Clark AG. 2011. The resolution of sexual antagonism by gene duplication. Genetics 187:919-937.
10. Conrad T, Akhtar A. 2011. Dosage compensation in Drosophila melanogaster: epigenetic fine-tuning of chromosome-wide transcription. Nat Rev Genet. 13:123-134.
11. Draghici S. 2012. Statistics and data analysis for microarrays using R and bioconductor. Boca Raton, FL: CRC Press.
12. Ellegren H, et al. 2007. Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes. BMC Biol. 5:40.
13. Frentiu FD, Adamski M, McGraw EA, Blows MW, Chenoweth SF. 2009. An expressed sequence tag (EST) library for Drosophila serrata, a model system for sexual selection and climatic adaptation studies. BMC Genomics 10:40.
14. Gallach M, Betran E. 2011. Intralocus sexual conflict resolved through gene duplication. Trends Ecol Evol. 26:222-228.
15. Gentleman RC, et al. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5:R80.
16. Gladstein N, McKeon MN, Horabin JI. 2010. Requirement of male-specific dosage compensation in Drosophila females-implications of early X chromosome gene expression. PLoS Genet. 6:e1001041.
17. Gupta V, et al. 2006. Global analysis of X-chromosome dosage compensation. J Biol. 5:3.
18. HanMV, Hahn MW. 2012. Inferring the history of interchromosomal gene transposition in Drosophila using n-dimensional parsimony. Genetics 190:813-825.
19. Hardy SJ. 1975. The stoichiometry of the ribosomal proteins of Escherichia coli. Mol Gen Genet. 140:253-274.
20. Hense W, Baines JF, Parsch J. 2007. X chromosome inactivation during Drosophila spermatogenesis. PLoS Biol. 5:e273.
21. Itoh Y, et al. 2010. Sex bias and dosage compensation in the zebra finch versus chicken genomes: general and specialized patterns among birds. Genome Res. 20:512-518.
22. Kaiser VB, Bachtrog D. 2010. Evolution of sex chromosomes in insects. Annu Rev Genet. 44:91-112.
23. Khil PP, Smirnova NA, Romanienko PJ, Camerini-Otero RD. 2004. The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat Genet. 36: 642-646.
24. Lande R. 1980. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34:292-305.
25. Lercher MJ, Urrutia AO, Hurst LD. 2003. Evidence that the human X chromosome is enriched for male-specific but not female-specific genes. Mol Biol Evol. 20:1113-1116.
26. Lindstrom MS. 2009. Emerging functions of ribosomal proteins in genespecific transcription and translation. Biochem Biophys Res Commun. 379:167-170.
27. Mank JE, Ellegren H. 2009. All dosage compensation is local: geneby-gene regulation of sex-biased expression on the chicken Z chromosome. Heredity (Edinb) 102:312-320.
28. Mank JE, Hultin-Rosenberg L, Webster MT, Ellegren H. 2008. The unique genomic properties of sex-biased genes: insights from avian microarray data. BMC Genomics 9:148.
29. Meiklejohn CD, Landeen EL, Cook JM, Kingan SB, Presgraves DC. 2011. Sex chromosome-specific regulation in the Drosophila male germline but little evidence for chromosomal dosage compensation or meiotic inactivation. PLoS Biol. 9:e1001126.
30. Meiklejohn CD, Presgraves DC. 2012. Little evidence for demasculinization of the Drosophila X chromosome among genes expressed in the male germline. Genome Biol Evol. 4:1007-1016.
31. Meisel RP, Malone JH, Clark AG. 2012. Disentangling the relationship between sex-biased gene expression and X-linkage. Genome Res. 22:1255-1265.
32. Mikhaylova LM, Nurminsky DI. 2011. Lack of global meiotic sex chromosome inactivation, and paucity of tissue-specific gene expression on the Drosophila X chromosome. BMC Biol. 9:29.
33. Ohno S. 1967. Sex chromosomes and sex-linked genes. Berlin, Heidelberg, New York: Springer-Verlag.
34. Parisi M, et al. 2003. Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science 299:697-700.
35. Pessia E, Makino T, Bailly-Bechet M, McLysaght A, Marais GA. 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.
36. 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.
37. Rice WR. 1984. Sex-chromosomes and the evolution of sexual dimorphism. Evolution 38:735-742.
38. Stocker AJ, et al. 2012. Physical and linkage maps for Drosophila serrata, a model species for studies of clinal adaptation and sexual selection. G3 (Bethesda) 2:287-297.
39. Sturgill D, Zhang Y, Parisi M, Oliver B. 2007. Demasculinization of X chromosomes in the Drosophila genus. Nature 450:238-241.
40. Tamura K, Subramanian S, Kumar S. 2004. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol. 21:36-44.
41. Vicoso B, Charlesworth B. 2009. The deficit of male-biased genes on the D. melanogaster X chromosome is expressiondependent: a consequence of dosage compensation? J Mol Evol. 68:576-583.
42. Voynow P, Kurland CG. 1971. Stoichiometry of the 30S ribosomal proteins of Escherichia coli. Biochemistry 10:517-524.
43. Wang PJ, McCarrey JR, Yang F, Page DC. 2001. An abundance of X-linked genes expressed in spermatogonia. Nat Genet. 27: 422-426.
44. Yanai I, et al. 2005. Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification. Bioinformatics 21:650-659.
45. Yang X, et al. 2006. Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res. 16:995-1004.
46. Zhang Y, Oliver B. 2010. An evolutionary consequence of dosage compensation on Drosophila melanogaster female X-chromatin structure? BMC Genomics 11:6.
47. Zhang Y, Sturgill D, Parisi M, Kumar S, Oliver B. 2007. Constraint and turnover in sex-biased gene expression in the genus Drosophila. Nature 450:233-237.
48. Zhou Q, Bachtrog D. 2012. Chromosome-wide gene silencing initiates Y degeneration in Drosophila. Curr Biol. 22:522-525.