Unifying Genetic Canalization, Genetic Constraint, and Genotype-by-Environment Interaction: QTL by Genomic Background by Environment Interaction of Flowering Time in

English version České info

Biological traits often display large amounts of genetic variability as well as genetic correlations among traits. This variability provides the raw material for evolutionary change and may alter the direction of trait evolution under selection. Despite this importance, it is unclear whether the genetic controls of variability in single traits and relationships among multiple traits have related mechanisms. Using the flowering time of a plant species as model, here we performed genetic mapping and identified a locus altering single-trait variability and multi-trait relationships. The effect likely results from the distinct thresholds required by its different alleles to trigger flowering, which can be explained by the interaction among this major locus, the variable genomic backgrounds, and the distinct environments. This view is supported by experiments showing epistatic effects of this major locus on flowering time and expression pattern of the candidate gene. Together, our results show that, at least for traits with major signal integrator genes such as flowering time, the genetic control of single-trait variability and multi-trait relationships may have a common underlying mechanism that may be generalizable to other genes or pathways, mediated by interaction among major loci, genomic backgrounds, and surrounding environments.

Vyšlo v časopise: Unifying Genetic Canalization, Genetic Constraint, and Genotype-by-Environment Interaction: QTL by Genomic Background by Environment Interaction of Flowering Time in. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004727
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004727

Souhrn

Zdroje

1. MackayTFC (2001) The Genetic Architecture Of Quantitative Traits. Annu Rev Genet 35: 303–339.

2. KellyJK (2009) CONNECTING QTLS TO THE G-MATRIX OF EVOLUTIONARY QUANTITATIVE GENETICS. Evolution 63: 813–825.

3. SteppanSJ, PhillipsPC, HouleD (2002) Comparative quantitative genetics: evolution of the G matrix. Trends Ecol Evol

4. ElenaSF, LenskiRE (2001) Epistasis between new mutations and genetic background and a test of genetic canalization. Evolution 55: 1746–1752.

5. MeiklejohnCD, HartlDL (2002) A single mode of canalization. Trends Ecol Evol 17: 468–473.

6. FlattT (2005) The evolutionary genetics of canalization. Q Rev Biol 80: 287–316.

7. HallMC, DworkinI, UngererMC, PuruggananM (2007) Genetics of microenvironmental canalization in Arabidopsis thaliana. Proc Natl Acad Sci U S A 104: 13717–13722.

8. ShenX, PetterssonM, RönnegårdL, CarlborgÖ (2012) Inheritance beyond plain heritability: variance-controlling genes in Arabidopsis thaliana. PLoS Genetics 8: e1002839.

9. Jimenez-GomezJM, CorwinJA, JosephB, MaloofJN, KliebensteinDJ (2011) Genomic analysis of QTLs and genes altering natural variation in stochastic noise. PLoS Genetics 7: e1002295.

10. AnselJ, BottinH, Rodriguez-BeltranC, DamonC, NagarajanM, et al. (2008) Cell-to-cell stochastic variation in gene expression is a complex genetic trait. PLoS Genetics 4: e1000049.

11. PerryGM, NehrkeKW, BushinskyDA, ReidR, LewandowskiKL, et al. (2012) Sex modifies genetic effects on residual variance in urinary calcium excretion in rat (Rattus norvegicus). Genetics 191: 1003–1013.

12. FraserHB, SchadtEE (2010) The quantitative genetics of phenotypic robustness. PLoS One 5: e8635.

13. YangJ, LoosRJF, PowellJE, MedlandSE, SpeliotesEK, et al. (2012) FTO genotype is associated with phenotypic variability of body mass index. Nature 490: 267–272.

14. HulseAM, CaiJJ (2013) Genetic variants contribute to gene expression variability in humans. Genetics 193: 95–108.

15. PareG, CookNR, RidkerPM, ChasmanDI (2010) On the use of variance per genotype as a tool to identify quantitative trait interaction effects: a report from the Women's Genome Health Study. PLoS Genet 6: e1000981.

16. WangG, YangE, Brinkmeyer-LangfordCL, CaiJJ (2014) Additive, Epistatic, and Environmental Effects Through the Lens of Expression Variability QTL in a Twin Cohort. Genetics 196: 413–425.

17. WagnerGP, BoothG, Bagheri-ChaichianH (1997) A population genetic theory of canalization. Evolution 329–347.

18. GibsonG, WagnerG (2000) Canalization in evolutionary genetics: a stabilizing theory? BioEssays 22: 372–380.

19. LandeR (1979) Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry. Evolution 33: 402–416.

20. De JongG (1995) Phenotypic plasticity as a product of selection in a variable environment. Am Nat 493–512.

21. FalconerDS (1952) The problem of environment and selection. Am Nat 293–298.

22. YamadaY (1962) Genotype by environment interaction and genetic correlation of the same trait under different environments. Jpn J Genet 37: 498–509.

23. ArnoldSJ (1992) Constraints on phenotypic evolution. Am Nat S85–S107.

24. ForrestJ, Miller-RushingAJ (2010) Toward a synthetic understanding of the role of phenology in ecology and evolution. Philos Trans R Soc Lond B Biol Sci 365: 3101–3112.

25. AndersonJT, LeeC-R, Mitchell-OldsT (2011) Life history QTLs and natural selection on flowering time in Boechera stricta, a perennial relative of Arabidopsis. Evolution 65: 771–787.

26. RushworthCA, SongB-H, LeeC-R, Mitchell-OldsT (2011) Boechera, a model system for ecological genomics. Mol Ecol 20: 4843–4857.

27. AndersonJT, LeeC-R, Mitchell-OldsT (2014) Strong selection genome-wide enhances fitness trade-offs across environments and episodes of selection. Evolution 68: 16–31.

28. AndersonJT, LeeC-R, RushworthC, ColauttiRI, Mitchell-OldsT (2012) Genetic tradeoffs and conditional neutrality contribute to local adaptation. Mol Ecol 22: 699–708.

29. RutherfordSL, LindquistS (1998) Hsp90 as a capacitor for morphological evolution. Nature 396: 336–342.

30. PinPA, NilssonO (2012) The multifaceted roles of FLOWERING LOCUS T in plant development. Plant Cell Environ 35: 1742–1755.

31. BoxGEP (1949) A general distribution theory for a class of likelihood criteria. Biometrika 317–346.

32. BlowsMW, ChenowethSF, HineE (2004) Orientation of the genetic variance-covariance matrix and the fitness surface for multiple male sexually selected traits. Am Nat 163: 329–340.

33. KrzanowskiWJ (1979) Between-groups comparison of principal components. Journal of the American Statistical Association 74: 703–707.

34. HuangW, RichardsS, CarboneMA, ZhuD, AnholtRRH, et al. (2012) Epistasis dominates the genetic architecture of Drosophila quantitative traits. Proc Natl Acad Sci 109: 15553–15559.

35. BreenMS, KemenaC, VlasovPK, NotredameC, KondrashovFA (2012) Epistasis as the primary factor in molecular evolution. Nature 490: 535–538.

36. KellyJK (2005) Epistasis in monkeyflowers. Genetics 171: 1917–1931.

37. CaicedoAL, StinchcombeJR, OlsenKM, SchmittJ, PuruggananMD (2004) Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proc Natl Acad Sci 101: 15670–15675.

38. CarlborgO, JacobssonL, AhgrenP, SiegelP, AnderssonL (2006) Epistasis and the release of genetic variation during long-term selection. Nat Genet 38: 418–420.

39. CarlborgO, HaleyCS (2004) Epistasis: too often neglected in complex trait studies? Nat Rev Genet 5: 618-U614.

40. CamargoL, OsbornT (1996) Mapping loci controlling flowering time in Brassica oleracea. Theor Appl Genet 92: 610–616.

41. SimpsonGG, DeanC (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296: 285–289.

42. WelchSM, RoeJL, DongZ (2003) A Genetic Neural Network Model of Flowering Time Control in Arabidopsis thaliana. Agron J 95: 71–81.

43. PaabyAB, RockmanMV (2014) Cryptic genetic variation: evolution's hidden substrate. Nat Rev Genet 247–58.

44. RohnerN, JaroszDF, KowalkoJE, YoshizawaM, JefferyWR, et al. (2013) Cryptic variation in morphological evolution: HSP90 as a capacitor for loss of eyes in cavefish. Science 342: 1372–1375.

45. SchlesingerMJ (1990) Heat shock proteins. J Biol Chem 265: 12111–12114.

46. WiechH, BuchnerJ, ZimmermannR, JakobU (1992) Hsp90 chaperones protein folding in vitro. Nature 358: 169–170.

47. Gething M-J, Sambrook J (1992) Protein folding in the cell.

48. SiegalML, BergmanA (2002) Waddington's canalization revisited: Developmental stability and evolution. PNAS 99: 10528–14660.

49. BergmanA, SiegalML (2003) Evolutionary capacitance as a general feature of complex gene networks. Nature 424: 549–552.

50. LevySF, SiegalML (2008) Network hubs buffer environmental variation in Saccharomyces cerevisiae. PLoS Biol 6: e264.

51. FinlayKW, WilkinsonGN (1963) The analysis of adaptation in a plant-breeding programme. Aust J Agric Res 14: 742–754.

52. StinchcombeJR, WeinigC, UngererM, OlsenKM, MaysC, et al. (2004) A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc Natl Acad Sci 101: 4712–4717.

53. ProulxSR, PhillipsPC (2005) The opportunity for canalization and the evolution of genetic networks. Am Nat 165: 147–162.

54. PetterssonME, NelsonRM, CarlborgÖ (2012) Selection On Variance-Controlling Genes: Adaptability or Stability. Evolution 66: 3945–3949.

55. StearnsSC, KaweckiTJ (1994) Fitness sensitivity and the canalization of life-history traits. Evolution 1438–1450.

56. StearnsSC, KaiserM, KaweckiTJ (1995) The differential genetic and environmental canalization of fitness components in Drosophila melanogaster. J Evol Biol 8: 539–557.

57. WadeMJ (2001) Epistasis, complex traits, and mapping genes. Genetica 112–113: 59–69.

58. ArnoldSJ, BürgerR, HohenlohePA, AjieBC, JonesAG (2008) Understanding the evolution and stability of the G-matrix. Evolution 62: 2451–2461.

59. StinchcombeJR, SimonsenAK, BlowsM (2013) ESTIMATING UNCERTAINTY IN MULTIVARIATE RESPONSES TO SELECTION. Evolution 68: 1188–1196.

60. AguirreJD, HineE, McGuiganK, BlowsMW (2014) Comparing G: multivariate analysis of genetic variation in multiple populations. Heredity 112: 21–29.

61. StinchcombeJR, WeinigC, HeathKD, BrockMT, SchmittJ (2009) Polymorphic Genes of Major Effect: Consequences for Variation, Selection and Evolution in Arabidopsis thaliana. Genetics 182: 911–922.

62. WolfJB, LeamyLJ, RoutmanEJ, CheverudJM (2005) Epistatic pleiotropy and the genetic architecture of covariation within early and late-developing skull trait complexes in mice. Genetics 171: 683–694.

63. DebatV, DavidP (2001) Mapping phenotypes: canalization, plasticity and developmental stability. Trends Ecol Evol 16: 555–561.

64. SgroCM, HoffmannAA (2004) Genetic correlations, tradeoffs and environmental variation. Heredity 93: 241–248.

65. Mendez-VigoB, Martinez-ZapaterJM, Alonso-BlancoC (2013) The flowering repressor SVP underlies a novel Arabidopsis thaliana QTL interacting with the genetic background. PLoS Genet 9: e1003289.

66. KorvesTM, SchmidKJ, CaicedoAL, MaysC, StinchcombeJR, et al. (2007) Fitness effects associated with the major flowering time gene FRIGIDA in Arabidopsis thaliana in the field. Am Nat 169: E141–E157.

67. BrownAA, BuilA, ViñuelaA, LappalainenT, ZhengH-F, et al. (2014) Genetic interactions affecting human gene expression identified by variance association mapping. eLife 3.

68. BeavisWD (1994) The power and deceit of QTL experiments: Lessons from comparative QTL studies. Proceedings of the forty-ninth annual corn and sorghum industry research conference 49: 250–266.

69. Beavis WD (1998) QTL analyses: power, precision, and accuracy. In: Paterson AH, editor. Molecular dissection of complex traits. Boca Raton: CRC Press. pp. 145–162.

70. XuSZ (2003) Theoretical basis of the Beavis effect. Genetics 165: 2259–2268.

71. TonsorSJ, ElnaccashTW, ScheinerSM (2013) Developmental instability is genetically correlated with phenotypic plasticity, constraining heritability, and fitness. Evolution 67: 2923–2935.

72. SchranzME, ManzanedaAJ, WindsorAJ, ClaussMJ, Mitchell-OldsT (2009) Ecological genomics of Boechera stricta: identification of a QTL controlling the allocation of methionine- vs branched-chain amino acid-derived glucosinolates and levels of insect herbivory. Heredity 102: 465–474.

73. ChurchillGA, DoergeRW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138: 963–971.

74. ValladaresF, Sanchez-GomezD, ZavalaMA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94: 1103–1116.

75. SchluterD (1996) Adaptive radiation along genetic lines of least resistance. Evolution 50: 1766–1774.

76. LeeC-R, Mitchell-OldsT (2013) Complex trait divergence contributes to environmental niche differentiation in ecological speciation of Boechera stricta. Mol Ecol 22: 2204–2217.

77. CorbesierL, VincentC, JangS, FornaraF, FanQ, et al. (2007) FT Protein Movement Contributes to Long-Distance Signaling in Floral Induction of Arabidopsis. Science 316: 1030–1033.

78. KimSY, YuX, MichaelsSD (2008) Regulation of CONSTANS and FLOWERING LOCUS T Expression in Response to Changing Light Quality. Plant Physiol 148: 269–279.

79. ChengXF, WangZY (2005) Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana. Plant J 43: 758–768.

80. YanovskyMJ, KaySA (2002) Molecular basis of seasonal time measurement in Arabidopsis. Nature 419: 308–312.

81. PrasadKVSK, SongBH, Olson-ManningC, AndersonJT, LeeCR, et al. (2012) A gain-of-function polymorphism controlling complex traits and fitness in nature. Science 337: 1081–1084.