Temperature Stress Mediates Decanalization and Dominance of Gene Expression in

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Gene expression is the most direct link between the genetically encoded information and the phenotype. We analyzed the patterns of gene expression in two different D. melanogaster genotypes and their offspring at four different temperatures to determine if gene expression regulation is modulated by temperature. Interestingly, we find that at the intermediate temperature (18°C) alleles from both genotypes have very similar gene expression, suggesting a strong canalization of gene expression despite substantial genetic differences. More extreme temperatures break this canalization and result in many differently expressed genes, caused mainly by trans-acting factors. Most of the expression differences are non-additive, with a swap in dominance between the two extreme temperatures.

Vyšlo v časopise: Temperature Stress Mediates Decanalization and Dominance of Gene Expression in. PLoS Genet 11(2): e32767. doi:10.1371/journal.pgen.1004883
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004883

Souhrn

Zdroje

1. Schmalhausen II (1949) Factors of Evolution: The Theory of Stabilizing Selection. Philadelphia: The Blankiston Company.

2. Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150: 563–565.

3. Siegal ML, Bergman A (2002) Waddington’s canalization revisited: developmental stability and evolution. Proc Natl Acad Sci U S A 99: 10528–10532. 12082173

4. Flatt T (2005) The evolutionary genetics of canalization. Q Rev Biol 80: 287–316. 16250465

5. Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396: 336–342. 9845070

6. Jarosz DF, Lindquist S (2010) Hsp90 and environmental stress transform the adaptive value of natural genetic variation. Science 330: 1820–1824. doi: 10.1126/science.1195487 21205668

7. Rohner N, Jarosz DF, Kowalko JE, Yoshizawa M, Jeffery WR, et al. (2013) Cryptic variation in morphological evolution: HSP90 as a capacitor for loss of eyes in cavefish. Science 342: 1372–1375. doi: 10.1126/science.1240276 24337296

8. Waddington CH (1953) Genetic assimilation of an acquired character. evolution 7: 118–126.

9. Waddington CH (1956) Genetic assimilation of the bithorax phenotype. evolution 10: 1–13.

10. Polaczyk PJ, Gasperini R, Gibson G (1998) Naturally occurring genetic variation affects Drosophila photoreceptor determination. Development Genes and Evolution 207: 462–470. 9510541

11. Gibson G, Hogness DS (1996) Effect of polymorphism in the Drosophila regulatory gene Ultrabithorax on homeotic stability. Science 271: 200–203. 8539619

12. Gavin-Smyth J, Wang YC, Butler I, Ferguson EL (2013) A genetic network conferring canalization to a bistable patterning system in Drosophila. Current Biology 23: 2296–2302. doi: 10.1016/j.cub.2013.09.055 24184102

13. Lott SE, Kreitman M, Palsson A, Alekseeva E, Ludwig MZ (2007) Canalization of segmentation and its evolution in Drosophila. Proc Natl Acad Sci U S A 104: 10926–10931. 17569783

14. Manu, Surkova S, Spirov AV, Gursky VV, Janssens H, et al. (2009) Canalization of gene expression in the Drosophila blastoderm by gap gene cross regulation. PLoS Biology 7: 591–603.

15. Marques-Pita M, Rocha LM (2013) Canalization and control in automata networks: body segmentation in Drosophila melanogaster. PLoS One 8.

16. Morris MR, Richard R, Leder EH, Barrett RD, Aubin-Horth N, et al. (2014) Gene expression plasticity evolves in response to colonization of freshwater lakes in threespine stickleback. Mol Ecol 23: 3226–3240. doi: 10.1111/mec.12820 24889067

17. Levine MT, Eckert ML, Begun DJ (2011) Whole-genome expression plasticity across tropical and temperate Drosophila melanogaster populations from Eastern Australia. Mol Biol Evol 28: 249–256. doi: 10.1093/molbev/msq197 20671040

18. Sikkink KL, Reynolds RM, Ituarte CM, Cresko WA, Phillips PC (2014) Rapid evolution of phenotypic plasticity and shifting thresholds of genetic assimilation in the nematode Caenorhabditis remanei. G3 (Bethesda) 4: 1103–1112. doi: 10.1534/g3.114.010553 24727288

19. Runcie DE, Garfield DA, Babbitt CC, Wygoda JA, Mukherjee S, et al. (2012) Genetics of gene expression responses to temperature stress in a sea urchin gene network. Mol Ecol 21: 4547–4562. doi: 10.1111/j.1365-294X.2012.05717.x 22856327

20. Yampolsky LY, Glazko GV, Fry JD (2012) Evolution of gene expression and expression plasticity in long-term experimental populations of Drosophila melanogaster maintained under constant and variable ethanol stress. Mol Ecol 21: 4287–4299. doi: 10.1111/j.1365-294X.2012.05697.x 22774776

21. Goncalves A, Leigh-Brown S, Thybert D, Stefflova K, Turro E, et al. (2012) Extensive compensatory cis-trans regulation in the evolution of mouse gene expression. Genome Research 22: 2376–2384. doi: 10.1101/gr.142281.112 22919075

22. Wittkopp PJ, Haerum BK, Clark AG (2004) Evolutionary changes in cis and trans gene regulation. Nature 430: 85–88. 15229602

23. Tirosh I, Reikhav S, Levy AA, Barkai N (2009) A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324: 659–662. doi: 10.1126/science.1169766 19407207

24. McManus CJ, Coolon JD, Duff MO, Eipper-Mains J, Graveley BR, et al. (2010) Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Research 20: 816–825. doi: 10.1101/gr.102491.109 20354124

25. Wittkopp PJ, Haerum BK, Clark AG (2006) Parent-of-origin effects on mRNA expression in Drosophila melanogaster not caused by genomic imprinting. Genetics 173: 1817–1821. 16702434

26. Menon DU, Meller VH (2010) Germ line imprinting in Drosophila: Epigenetics in search of function. Fly (Austin) 4: 48–52. 20081359

27. Coolon JD, Stevenson KR, McManus CJ, Graveley BR, Wittkopp PJ (2012) Genomic imprinting absent in Drosophila melanogaster adult females. Cell Reports 2: 69–75. doi: 10.1016/j.celrep.2012.06.013 22840398

28. Li Y, Alvarez OA, Gutteling EW, Tijsterman M, Fu J, et al. (2006) Mapping determinants of gene expression plasticity by genetical genomics in C. elegans. PLoS Genet 2: e222. 17196041

29. Smith EN, Kruglyak L (2008) Gene-environment interaction in yeast gene expression. PLoS Biol 6: e83. doi: 10.1371/journal.pbio.0060083 18416601

30. Delpuech JM, Moreteau B, Chiche J, Pla E, Vouidibio J, et al. (1995) Phenotypic plasticity and reaction norms in temperate and tropical populations of Drosophila melanogaster ovarian size and developmental temperature. evolution 49: 670–675.

31. Klepsatel P, Galikova M, De Maio N, Ricci S, Schlötterer C, et al. (2013) Reproductive and post-reproductive life history of wild-caught Drosophila melanogaster under laboratory conditions. Journal of Evolutionary Biology 26: 1508–1520. doi: 10.1111/jeb.12155 23675912

32. Shen WL, Kwon Y, Adegbola AA, Luo JJ, Chess A, et al. (2011) Function of Rhodopsin in Temperature Discrimination in Drosophila. Science 331: 1333–1336. doi: 10.1126/science.1198904 21393546

33. Kwon Y, Shim HS, Wang XY, Montell C (2008) Control of thermotactic behavior via coupling of a TRP channel to a phospholipase C signaling cascade. Nature Neuroscience 11: 871–873. doi: 10.1038/nn.2170 18660806

34. Lindsley DL, Grell EH (1968) Genetic variations of Drosophila melanogaster. Washington, D.C.: Carnegie Institute of Washington Publication.

35. Jin W, Riley RM, Wolfinger RD, White KP, Passador-Gurgel G, et al. (2001) The contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster. Nat Genet 29: 389–395. 11726925

36. King EG, Sanderson BJ, McNeil CL, Long AD, Macdonald SJ (2014) Genetic dissection of the Drosophila melanogaster female head transcriptome reveals widespread allelic heterogeneity. PLoS Genet 10: e1004322. doi: 10.1371/journal.pgen.1004322 24810915

37. Gibson G (2009) Decanalization and the origin of complex disease. Nature Reviews Genetics 10: 134–140. doi: 10.1038/nrg2502 19119265

38. Ezzati M, Lopez AD (2003) Estimates of global mortality attributable to smoking in 2000. Lancet 362: 847–852. 13678970

39. Ge B, Pokholok DK, Kwan T, Grundberg E, Morcos L, et al. (2009) Global patterns of cis variation in human cells revealed by high-density allelic expression analysis. Nature Genetics 41: 1216–U1278. doi: 10.1038/ng.473 19838192

40. Emilsson V, Thorleifsson G, Zhang B, Leonardson AS, Zink F, et al. (2008) Genetics of gene expression and its effect on disease. Nature 452: 423–U422. doi: 10.1038/nature06758 18344981

41. Mondal AK, Sharma NK, Elbein SC, Das SK (2013) Allelic expression imbalance screening of genes in chromosome 1q21–24 region to identify functional variants for Type 2 diabetes susceptibility. Physiological Genomics 45: 509–520. doi: 10.1152/physiolgenomics.00048.2013 23673729

42. Verlaan DJ, Berlivet S, Hunninghake GM, Madore AM, Lariviere M, et al. (2009) Allele-specific chromatin remodeling in the ZPBP2/GSDMB/ORMDL3 locus associated with the risk of asthma and autoimmune disease. American Journal of Human Genetics 85: 377–393. doi: 10.1016/j.ajhg.2009.08.007 19732864

43. True HL, Lindquist SL (2000) A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407: 477–483. 11028992

44. Gibson G, vanHelden S (1997) Is function of the Drosophila homeotic gene Ultrabithorax canalized? Genetics 147: 1155–1168. 9383059

45. Richardson JB, Uppendahl LD, Traficante MK, Levy SF, Siegal ML (2013) Histone variant HTZ1 shows extensive epistasis with, but does not increase robustness to, new mutations. PLoS Genetics 9.

46. Suvorov A, Nolte V, Pandey RV, Franssen SU, Futschik A, et al. (2013) Intra-Specific regulatory variation in Drosophila pseudoobscura. Plos One 8.

47. Schaefke B, Emerson JJ, Wang TY, Lu MYJ, Hsieh LC, et al. (2013) Inheritance of gene expression level and selective constraints on trans- and cis-regulatory changes in yeast. Molecular Biology and Evolution 30: 2121–2133. doi: 10.1093/molbev/mst114 23793114

48. Zhang X, Cal AJ, Borevitz JO (2011) Genetic architecture of regulatory variation in Arabidopsis thaliana. Genome Res 21: 725–733. doi: 10.1101/gr.115337.110 21467266

49. Wayne ML, Korol A, Mackay TF (2005) Microclinal variation for ovariole number and body size in Drosophila melanogaster in ‘Evolution Canyon’. Genetica 123: 263–270. 15954497

50. Cali BM, Anderson P (1998) mRNA surveillance mitigates genetic dominance in Caenorhabditis elegans. Mol Gen Genet 260: 176–184. 9862469

51. Mellert DJ, Truman JW (2012) Transvection is common throughout the Drosophila genome. Genetics 191: 1129–U1130. doi: 10.1534/genetics.112.140475 22649078

52. Henikoff S, Comai L (1998) Trans-sensing effects: The ups and downs of being together. Cell 93: 329–332. 9590167

53. Chen JL, Huisinga KL, Viering MM, Ou SA, Wu CT, et al. (2002) Enhancer action in trans is permitted throughout the Drosophila genome. Proc Natl Acad Sci U S A 99: 3723–3728. 11904429

54. Johnston RJ, Desplan C (2014) Interchromosomal communication coordinates intrinsically stochastic expression between alleles. Science 343: 661–665. doi: 10.1126/science.1243039 24503853

55. Kofler R, Orozco-terWengel P, De Maio N, Pandey RV, Nolte V, et al. (2011) PoPoolation: A toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS One 6.

56. Wu TD, Watanabe CK (2005) GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21: 1859–1875. 15728110

57. Wu TD, Nacu S (2010) Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26: 873–881. doi: 10.1093/bioinformatics/btq057 20147302

58. Pandey RV, Franssen SU, Futschik A, Schlötterer C (2013) Allelic imbalance metre (Allim), a new tool for measuring allele-specific gene expression with RNA-seq data. Molecular Ecology Resources 13: 740–745. doi: 10.1111/1755-0998.12110 23615333

59. Marygold SJ, Leyland PC, Seal RL, Goodman JL, Thurmond J, et al. (2013) FlyBase: improvements to the bibliography. Nucleic Acids Research 41: D751–D757. doi: 10.1093/nar/gks1024 23125371

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

61. Robinson MD, Oshlack A (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biology 11.

62. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140. doi: 10.1093/bioinformatics/btp616 19910308

63. McCarthy DJ, Chen YS, Smyth GK (2012) Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Research 40: 4288–4297. doi: 10.1093/nar/gks042 22287627

64. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Methodological 57: 289–300.

65. Terada A, Okada-Hatakeyama M, Tsuda K, Sese J (2013) Statistical significance of combinatorial regulations. Proc Natl Acad Sci U S A 110: 12996–13001. doi: 10.1073/pnas.1302233110 23882073

66. Murali T, Pacifico S, Yu JK, Guest S, Roberts GG, et al. (2011) DroID 2011: a comprehensive, integrated resource for protein, transcription factor, RNA and gene interactions for Drosophila. Nucleic Acids Research 39: D736–D743. doi: 10.1093/nar/gkq1092 21036869

67. Prüfer K, Muetzel B, Do HH, Weiss G, Khaitovich P, et al. (2007) FUNC: a package for detecting significant associations between gene sets and ontological annotations. BMC Bioinformatics 8.

68. Luo WJ, Friedman MS, Shedden K, Hankenson KD, Woolf PJ (2009) GAGE: generally applicable gene set enrichment for pathway analysis. BMC Bioinformatics 10.