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Sex Bias and Maternal Contribution to Gene Expression Divergence in Blastoderm Embryos


The early embryonic stage of development is unique as this stage begins under the genetic control of the mother and transitions to genetic control of the zygote. In order to investigate how these developmental specificities have shaped gene expression evolution, we studied the contribution of maternal gene expression to the pool of transcripts in the early embryo and how gene expression differs in early female and male embryos. We find extensive female-bias in gene expression, something not observed in adults. This is largely due to the delay in the establishment of a mechanism that balances gene expression from the differing number of X chromosomes in females and males. The maternal contribution to the transcript pool in the embryo is largely conserved over species, with some exceptions. However, there may also be some species-specific differences in the degradation rate of maternal transcripts, an often-overlooked contributor to variation in transcript level.


Vyšlo v časopise: Sex Bias and Maternal Contribution to Gene Expression Divergence in Blastoderm Embryos. PLoS Genet 11(10): e32767. doi:10.1371/journal.pgen.1005592
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005592

Souhrn

The early embryonic stage of development is unique as this stage begins under the genetic control of the mother and transitions to genetic control of the zygote. In order to investigate how these developmental specificities have shaped gene expression evolution, we studied the contribution of maternal gene expression to the pool of transcripts in the early embryo and how gene expression differs in early female and male embryos. We find extensive female-bias in gene expression, something not observed in adults. This is largely due to the delay in the establishment of a mechanism that balances gene expression from the differing number of X chromosomes in females and males. The maternal contribution to the transcript pool in the embryo is largely conserved over species, with some exceptions. However, there may also be some species-specific differences in the degradation rate of maternal transcripts, an often-overlooked contributor to variation in transcript level.


Zdroje

1. Lott SE, Villalta JE, Schroth GP, Luo S, Tonkin LA, et al. (2011) Noncanonical compensation of zygotic X transcription in early Drosophila melanogaster development revealed through single-embryo RNA-seq. PLoS Biol 9: e1000590. doi: 10.1371/journal.pbio.1000590 21346796

2. Lott SE, Villalta JE, Zhou Q, Bachtrog D, Eisen MB (2014) Sex-specific embryonic gene expression in species with newly evolved sex chromosomes. PLoS Genet 10: e1004159. doi: 10.1371/journal.pgen.1004159 24550743

3. Tadros W, Lipshitz HD (2009) The maternal-to-zygotic transition: a play in two acts. Development 136: 3033–3042. doi: 10.1242/dev.033183 19700615

4. Ellegren H, Parsch J (2007) The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet 8: 689–698. 17680007

5. Haerty W, Jagadeeshan S, Kulathinal RJ, Wong A, Ravi Ram K, et al. (2007) Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics 177: 1321–1335. 18039869

6. Meisel RP, Malone JH, Clark AG (2012) Disentangling the relationship between sex-biased gene expression and X-linkage. Genome Res 22: 1255–1265. doi: 10.1101/gr.132100.111 22499666

7. Ranz JM, Castillo-Davis CI, Meiklejohn CD, Hartl DL (2003) Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300: 1742–1745. 12805547

8. 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. 17994089

9. Arbeitman MN, Fleming AA, Siegal ML, Null BH, Baker BS (2004) A genomic analysis of Drosophila somatic sexual differentiation and its regulation. Development 131: 2007–2021. 15056610

10. Parisi M, Nuttall R, Edwards P, Minor J, Naiman D, et al. (2004) A survey of ovary-, testis-, and soma-biased gene expression in Drosophila melanogaster adults. Genome Biol 5: R40. 15186491

11. Meisel RP (2011) Towards a more nuanced understanding of the relationship between sex-biased gene expression and rates of protein-coding sequence evolution. Mol Biol Evol 28: 1893–1900. doi: 10.1093/molbev/msr010 21239389

12. Franke A, Dernburg A, Bashaw GJ, Baker BS (1996) Evidence that MSL-mediated dosage compensation in Drosophila begins at blastoderm. Development 122: 2751–2760. 8787749

13. Rastelli L, Richman R, Kuroda MI (1995) The dosage compensation regulators MLE, MSL-1 and MSL-2 are interdependent since early embryogenesis in Drosophila. Mech Dev 53: 223–233. 8562424

14. Strukov YG, Sural TH, Kuroda MI, Sedat JW (2011) Evidence of activity-specific, radial organization of mitotic chromosomes in Drosophila. PLoS Biol 9: e1000574. doi: 10.1371/journal.pbio.1000574 21264350

15. Kuntz SG, Eisen MB (2014) Drosophila embryogenesis scales uniformly across temperature in developmentally diverse species. PLoS Genet 10: e1004293. doi: 10.1371/journal.pgen.1004293 24762628

16. Markow TA, Beall S, Matzkin LM (2009) Egg size, embryonic development time and ovoviviparity in Drosophila species. J Evol Biol 22: 430–434. doi: 10.1111/j.1420-9101.2008.01649.x 19032497

17. Markow TA (2013) Parents without Partners: Drosophila as a Model for Understanding the Mechanisms and Evolution of Parthenogenesis. G3 (Bethesda).

18. Russo CA, Takezaki N, Nei M (1995) Molecular phylogeny and divergence times of drosophilid species. Mol Biol Evol 12: 391–404. 7739381

19. Paris M, Kaplan T, Li XY, Villalta JE, Lott SE, et al. (2013) Extensive divergence of transcription factor binding in Drosophila embryos with highly conserved gene expression. PLoS Genet 9: e1003748. doi: 10.1371/journal.pgen.1003748 24068946

20. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359. doi: 10.1038/nmeth.1923 22388286

21. Roberts A, Pachter L (2013) Streaming fragment assignment for real-time analysis of sequencing experiments. Nat Methods 10: 71–73. doi: 10.1038/nmeth.2251 23160280

22. Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, et al. (2011) The developmental transcriptome of Drosophila melanogaster. Nature 471: 473–479. doi: 10.1038/nature09715 21179090

23. Kalinka AT, Varga KM, Gerrard DT, Preibisch S, Corcoran DL, et al. (2010) Gene expression divergence recapitulates the developmental hourglass model. Nature 468: 811–814. doi: 10.1038/nature09634 21150996

24. Kaiser VB, Bachtrog D (2010) Evolution of sex chromosomes in insects. Annu Rev Genet 44: 91–112. doi: 10.1146/annurev-genet-102209-163600 21047257

25. Meisel RP, Malone JH, Clark AG (2012) Faster-X evolution of gene expression in Drosophila. PLoS Genet 8: e1003013. doi: 10.1371/journal.pgen.1003013 23071459

26. Kayserili MA, Gerrard DT, Tomancak P, Kalinka AT (2012) An excess of gene expression divergence on the X chromosome in Drosophila embryos: implications for the faster-X hypothesis. PLoS Genet 8: e1003200. doi: 10.1371/journal.pgen.1003200 23300473

27. Parisi M, Nuttall R, Naiman D, Bouffard G, Malley J, et al. (2003) Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science 299: 697–700. 12511656

28. Sturgill D, Zhang Y, Parisi M, Oliver B (2007) Demasculinization of X chromosomes in the Drosophila genus. Nature 450: 238–241. 17994090

29. Assis R, Zhou Q, Bachtrog D (2012) Sex-biased transcriptome evolution in Drosophila. Genome Biol Evol 4: 1189–1200. doi: 10.1093/gbe/evs093 23097318

30. Charlesworth B, Coyne JA, Barton NH (1987) The Relative Rates of Evolution of Sex Chromosomes and Autosomes. The American Naturalist 130: 113–146.

31. Meisel RP, Connallon T (2013) The faster-X effect: integrating theory and data. Trends Genet 29: 537–544. doi: 10.1016/j.tig.2013.05.009 23790324

32. Vicoso B, Charlesworth B (2006) Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet 7: 645–653. 16847464

33. Presgraves DC (2008) Sex chromosomes and speciation in Drosophila. Trends Genet 24: 336–343. doi: 10.1016/j.tig.2008.04.007 18514967

34. Avila V, Marion de Proce S, Campos JL, Borthwick H, Charlesworth B, et al. (2014) Faster-X effects in two Drosophila lineages. Genome Biol Evol 6: 2968–2982. doi: 10.1093/gbe/evu229 25323954

35. De Renzis S, Elemento O, Tavazoie S, Wieschaus EF (2007) Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol 5: e117. 17456005

36. Boettiger AN (2013) Analytic approaches to stochastic gene expression in multicellular systems. Biophys J 105: 2629–2640. doi: 10.1016/j.bpj.2013.10.033 24359735

37. Bolouri H, Davidson EH (2003) Transcriptional regulatory cascades in development: initial rates, not steady state, determine network kinetics. Proc Natl Acad Sci U S A 100: 9371–9376. 12883007

38. Cacace F, Paci P, Cusimano V, Germani A, Farina L (2012) Stochastic modeling of expression kinetics identifies messenger half-lives and reveals sequential waves of co-ordinated transcription and decay. PLoS Comput Biol 8: e1002772. doi: 10.1371/journal.pcbi.1002772 23144606

39. Elkon R, Zlotorynski E, Zeller KI, Agami R (2010) Major role for mRNA stability in shaping the kinetics of gene induction. BMC Genomics 11: 259. doi: 10.1186/1471-2164-11-259 20409322

40. Manu, Surkova S, Spirov AV, Gursky VV, Janssens H, et al. (2009) Canalization of gene expression and domain shifts in the Drosophila blastoderm by dynamical attractors. PLoS Comput Biol 5: e1000303. doi: 10.1371/journal.pcbi.1000303 19282965

41. Dori-Bachash M, Shema E, Tirosh I (2011) Coupled evolution of transcription and mRNA degradation. PLoS Biol 9: e1001106. doi: 10.1371/journal.pbio.1001106 21811398

42. Dillies MA, Rau A, Aubert J, Hennequet-Antier C, Jeanmougin M, et al. (2013) A comprehensive evaluation of normalization methods for Illumina high-throughput RNA sequencing data analysis. Brief Bioinform 14: 671–683. doi: 10.1093/bib/bbs046 22988256

43. R Core Team (2012) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.

44. Felsenstein J (1973) Maximum-likelihood estimation of evolutionary trees from continuous characters. Am J Hum Genet 25: 471–492. 4741844

45. Paradis E, Claude J, Strimmer K (2004) APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20: 289–290. 14734327

46. Meyer D, Dimitriadou E, Hornik K, Weingessel A, Leisch F (2014) e1071: Misc Functions of the Department of Statistics, TU Wien. R package version 1.6–4. ed.

47. Drosophila 12 Genomes C, Clark AG, Eisen MB, Smith DR, Bergman CM, et al. (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203–218. 17994087

48. Carvalho AB, Clark AG (2005) Y chromosome of D. pseudoobscura is not homologous to the ancestral Drosophila Y. Science 307: 108–110. 15528405

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