Inheritance Beyond Plain Heritability: Variance-Controlling Genes in

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The phenotypic effect of a gene is normally described by the mean-difference between alternative genotypes. A gene may, however, also influence the phenotype by causing a difference in variance between genotypes. Here, we reanalyze a publicly available Arabidopsis thaliana dataset [1] and show that genetic variance heterogeneity appears to be as common as normal additive effects on a genomewide scale. The study also develops theory to estimate the contributions of variance differences between genotypes to the phenotypic variance, and this is used to show that individual loci can explain more than 20% of the phenotypic variance. Two well-studied systems, cellular control of molybdenum level by the ion-transporter MOT1 and flowering-time regulation by the FRI-FLC expression network, and a novel association for Leaf serration are used to illustrate the contribution of major individual loci, expression pathways, and gene-by-environment interactions to the genetic variance heterogeneity.

Vyšlo v časopise: Inheritance Beyond Plain Heritability: Variance-Controlling Genes in. PLoS Genet 8(8): e32767. doi:10.1371/journal.pgen.1002839
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002839

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Zdroje

1. AtwellS, HuangYS, VilhjálmssonBJ, WillemsG, HortonM, et al. (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465: 627–631.

2. DworkinI (2005) Canalization, cryptic variation, and developmental buffering: A critical examination and analytical perspective. Review Literature And Arts Of The Americas Chapter 8 in: Variation 131–158.

3. HillWG, MulderH (2010) Genetic analysis of environmental variation. Genetics Research, Cambridge 92: 381–395.

4. KitanoH (2004) Biological robustness. Nature Reviews Genetics 5: 826–837.

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

6. DworkinI, PalssonA, BirdsallK, GibsonG (2003) Evidence that Egfr contributes to cryptic genetic variation for photoreceptor determination in natural populations of Drosophila melanogaster. Current Biology 13: 1888–1893.

7. MackayTF, LymanRF (2005) Drosophila bristles and the nature of quantitative genetic variation. Philosophical Transactions of the Royal Society, Series B 360: 1513–1527.

8. WellerJI, SollerM, BrodyT (1988) Linkage analysis of quantitative traits in an interspecific cross of tomato (Lycopersicon esculentum × Lycopersicon pimpinellifolium) by means of genetic markers. Genetics 118: 329–339.

9. HallMC, DworkinI, UngererMC, PuruggananM (2007) Genetics of microenvironmental canalization in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 104: 13717–13722.

10. OrdasB, MalvarRA, HillWG (2008) Genetic variation and quantitative trait loci associated with developmental stability and the environmental correlation between traits in maize. Genetics Research, Cambridge 90: 385–395.

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

12. FraserH, SchadtE (2010) The quantitative genetics of phenotypic robustness. PLoS ONE 5: e8635.

13. DengWQ, ParéG (2011) A fast algorithm to optimize SNP prioritization for gene-gene and geneenvironment interactions. Genetic Epidemiology 35: 729–38.

14. RönnegårdL, ValdarW (2011) Detecting major genetic loci controlling phenotypic variability in experimental crosses. Genetics 188: 435–447.

15. ParéG, 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 Genetics 6: e1000981.

16. StruchalinMV, DehghanA, WittemanJCM, DuijnCV, AulchenkoYS (2010) Variance heterogeneity analysis for detection of potentially interacting genetic loci: method and its limitations. BMC Genetics 11: 92.

17. ZhangX, HillWG (2005) Genetic variability under mutation selection balance. Trends in Ecology and Evolution 20: 468–470.

18. ZhangX (2005) Evolution and maintenance of the environmental component of the phenotypic variance: Benefit of plastic traits under changing environments. The American Naturalist 166: 569–580.

19. ZhangX, HillWG (2005) Evolution of the environmental component of the phenotypic variance: stabilizing selection in changing environments and the cost of homogeneity. Evolution 59: 1237–1244.

20. ZhangX, HillWG (2008) Mutation-selection balance for environmental variance. The American Naturalist 171: 394–399.

21. DevlinB, RoederK (1999) Genomic control for association studies. Biometrics 55: 997–1004.

22. KangHM, ZaitlenNA, WadeCM, KirbyA, HeckermanD, et al. (2008) Efficient control of population structure in model organism association mapping. Genetics 178: 1709–23.

23. KangHM, SulJH, ServiceSK, ZaitlenNA, KongSY, et al. (2010) Variance component model to account for sample structure in genome-wide association studies. Nature Genetics 42: 348–54.

24. TomatsuH, TakanoJ, TakahashiH, Watanabe-TakahashiA, ShibagakiN, et al. (2007) An Ara-bidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil. Proceedings of the National Academy of Sciences, USA 104: 18807–18812.

25. BaxterI, MuthukumarB, ParkHC, BuchnerP, LahnerB, et al. (2008) Variation in molybdenum content across broadly distributed populations of Arabidopsis thaliana is controlled by a mitochondrial molybdenum transporter (MOT1). PLoS Genetics 4: e1000004.

26. AndersonKV, InghamPW (2003) The transformation of the model organism: a decade of developmental genetics. Nature Genetics 33: Suppl 285–293.

27. FreemanM (2000) Signalling in development. Nature 408: 313–319.

28. BecskeiA, SerranoL (2000) Engineering stability in gene networks by autoregulation. Nature 405: 590–593.

29. SeoE, LeeH, JeonJ, ParkH, KimJ, et al. (2009) Crosstalk between cold response and owering in Arabidopsis is mediated through the owering-time gene SOC1 and its upstream negative regulator FLC. The Plant Cell 21: 3185–3197.

30. MichaelsS, AmasinoR (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of owering. The Plant Cell 11: 949–956.

31. DevauxC, LandeR (2010) Selection on variance in owering time within and among individuals. Evolution 64: 1311–1320.

32. ShindoC, AranzanaMJ, ListerC, BaxterC, NichollsC, et al. (2005) Role of FRIGIDA and FLOWERING LOCUS C in determining variation in owering time of arabidopsis. Plant Physiology 138: 1163–1173.

33. ConteM, de SimoneS, SimmonsSJ, BallaréCL, StapletonAE (2010) Chromosomal loci important for cotyledon opening under UV-B in Arabidopsis thaliana. BMC Plant Biology 10: 112.

34. PriceTD, QvarnströmA, IrwinDE (2003) The role of phenotypic plasticity in driving genetic evolution. Proceedings of the Royal Society, Series B 270: 1433–40.

35. HaldaneJ (1930) A mathematical theory of natural and artificial selection. vii. selection intensity as a function of mortality rate. Mathematical Proceedings of the Cambridge Philosophical Society 27: 131–136.

36. AulchenkoY, RipkeS, IsaacsA, van DuijnC (2007) GenABEL: an R package for genome-wide association analysis. Bioinformatics 23: 1294–1296.

37. GrennanA (2006) Variations on a theme. regulation of owering time in Arabidopsis. Plant Physiology 140: 399–400.