Powerful decomposition of complex traits in a diploid model

Nature Communications

Volumn 7, Issue , 2016, Pages

  Hallin, Johan ^a   Märtens, Kaspar ^b   Young, Alexander I ^c   Zackrisson, Martin ^d   Salinas, Francisco ^a,g   Parts, Leopold ^b,e   Warringer, Jonas ^d,f   Liti, Gianni ^a  

^a UNIVERSITY OF NICE SOPHIA ANTIPOLIS   (France)

^b UNIVERSITY OF TARTU   (Estonia)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^f NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^g PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

EPISTASIS; FITNESS; GENOME; HERITABILITY; HETEROSIS; HYBRID; PLEIOTROPY; YEAST;

DECOMPOSITION; DIPLOIDY; EPISTASIS; GAMETE; GENETIC MODEL; GENOME; HERITABILITY; HETEROSIS; NONHUMAN; OUTBRED STRAIN; PLEIOTROPY; QUANTITATIVE TRAIT LOCUS; SACCHAROMYCES CEREVISIAE; BIOLOGICAL MODEL; CHROMOSOMAL MAPPING; GENETICS; HYBRIDIZATION; QUANTITATIVE TRAIT;

SACCHAROMYCES CEREVISIAE;

CHROMOSOME MAPPING; DIPLOIDY; HYBRID VIGOR; HYBRIDIZATION, GENETIC; MODELS, GENETIC; QUANTITATIVE TRAIT LOCI; QUANTITATIVE TRAIT, HERITABLE; SACCHAROMYCES CEREVISIAE;

EID: 84994259847     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms13311     Document Type: Article

References (58)

1. Visscher, P. M., Brown, M. A., McCarthy, M. I. & Yang, J. Five years of GWAS discovery. Am. J. Hum. Genet. 90, 7-24 (2012).
2. Eichler, E. E. et al. Missing heritability and strategies for finding the underlying causes of complex disease. Nat. Rev. Genet. 11, 446-450 (2010).
3. Yang, J. et al. Common SNPs explain a large proportion of the heritability for human height. Nat. Genet. 42, 565-569 (2010).
4. Lehner, B. Molecular mechanisms of epistasis within and between genes. Trends Genet. 27, 323-331 (2011).
5. Zuk, O., Hechter, E., Sunyaev, S. R. & Lander, E. S. The mystery of missing heritability: genetic interactions create phantom heritability. Proc. Natl. Acad. Sci. USA 109, 1193-1198 (2012).
6. Abney, M., McPeek, M. S. & Ober, C. Estimation of variance components of quantitative traits in inbred populations. Am. J. Hum. Genet. 66, 629-650 (2000).
7. Lehner, B. Genotype to phenotype: lessons from model organisms for human genetics. Nat. Rev. Genet. 14, 168-178 (2013).
8. Liti, G. & Schacherer, J. The rise of yeast population genomics. C. R. Biol. 334, 612-619 (2011).
9. Hancock, J. M. et al. Phenomics (CRC Press, 2014).
10. Bloom, J. S. et al. Genetic interactions contribute less than additive effects to quantitative trait variation in yeast. Nat. Commun. 6, 8712-8716 (2015).
11. Bloom, J. S., Ehrenreich, I. M., Loo, W. T., Lite, T.-L. V. & Kruglyak, L. Finding the sources of missing heritability in a yeast cross. Nature 494, 234-237 (2013).
12. Young, A. I. & Durbin, R. Estimation of epistatic variance components and heritability in founder populations and crosses. Genetics 198, 1405-1416 (2014).
13. Threadgill, D. W., Hunter, K. W. & Williams, R. W. Genetic dissection of complex and quantitative traits: from fantasy to reality via a community effort. Mamm. Genome 13, 175-178 (2002).
14. Tsaih, S.-W., Lu, L., Airey, D. C., Williams, R. W. & Churchill, G. A. Quantitative trait mapping in a diallel cross of recombinant inbred lines. Mamm. Genome 16, 344-355 (2005).
15. Zou, F. et al. Quantitative trait locus analysis using recombinant inbred intercrosses: theoretical and empirical considerations. Genetics 170, 1299-1311 (2005).
16. Parts, L. et al. Revealing the genetic structure of a trait by sequencing a population under selection. Genome Res. 21, 1131-1138 (2011).
17. Cubillos, F. A. et al. High-resolution mapping of complex traits with a fourparent advanced intercross yeast population. Genetics 195, 1141-1155 (2013).
18. Illingworth, C. J. R., Parts, L., Bergström, A., Liti, G. & Mustonen, V. Inferring genome-wide recombination landscapes from advanced intercross lines: application to yeast crosses. PLoS ONE 8, e62266 (2013).
19. Märtens, K., Hallin, J., Warringer, J., Liti, G. & Parts, L. Predicting quantitative traits from genome and phenome with near perfect accuracy. Nat. Commun. 7, 11512 (2016).
20. Zackrisson, M. et al. Scan-o-matic: High-Resolution Microbial Phenomics at a Massive Scale. G3 (Bethesda) 6, 3003-3014 (2016).
21. Warringer, J. et al. Trait variation in yeast is defined by population history. PLoS Genet. 7, e1002111 (2011).
22. Ibstedt, S. et al. Concerted evolution of life stage performances signals recent selection on yeast nitrogen use. Mol. Biol. Evol. 32, 153-161 (2015).
23. Warringer, J., Anevski, D., Liu, B. & Blomberg, A. Chemogenetic fingerprinting by analysis of cellular growth dynamics. BMC Chem. Biol. 8, 3 (2008).
24. Joshi, P. K. et al. Directional dominance on stature and cognition in diverse human populations. Nature 523, 459-462 (2015).
25. Magwene, P. M. et al. Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 108, 1987-1992 (2011).
26. Wang, Q.-M., Liu, W.-Q., Liti, G., Wang, S.-A. & Bai, F.-Y. Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity. Mol. Ecol. 21, 5404-5417 (2012).
27. Bergström, A. et al. A high-definition view of functional genetic variation from natural yeast genomes. Mol. Biol. Evol. 31, 872-888 (2014).
28. Cubillos, F. A. et al. Assessing the complex architecture of polygenic traits in diverged yeast populations. Mol. Ecol. 20, 1401-1413 (2011).
29. Plech, M., de Visser, J. A. G. M. & Korona, R. Heterosis is prevalent among domesticated but not wild strains of Saccharomyces cerevisiae. G3 (Bethesda) 4, 315-323 (2014).
30. Zörgö, E. et al. Life history shapes trait heredity by accumulation of loss-offunction alleles in yeast. Mol. Biol. Evol. 29, 1781-1789 (2012).
31. Shapira, R., Levy, T., Shaked, S., Fridman, E. & David, L. Extensive heterosis in growth of yeast hybrids is explained by a combination of genetic models. Heredity (Edinb) 113, 316-326 (2014).
32. Ehrenreich, I. M. et al. Dissection of genetically complex traits with extremely large pools of yeast segregants. Nature 464, 1039-1042 (2010).
33. Lorenz, K. & Cohen, B. A. Small- and large-effect quantitative trait locus interactions underlie variation in yeast sporulation efficiency. Genetics 192, 1123-1132 (2012).
34. Zörgö, E. et al. Ancient evolutionary trade-offs between yeast ploidy states. PLoS Genet. 9, e1003388 (2013).
35. Gerstein, A. C. & Berman, J. Shift and adapt: the costs and benefits of karyotype variations. Curr. Opin. Microbiol. 26, 130-136 (2015).
36. Gerstein, A. C. & Otto, S. P. Ploidy and the causes of genomic evolution. J. Hered. 100, 571-581 (2009).
37. Chaisson, M. J. P., Wilson, R. K. & Eichler, E. E. Genetic variation and the de novo assembly of human genomes. Nat. Rev. Genet. 16, 627-640 (2015).
38. Perlstein, E. O., Ruderfer, D. M., Roberts, D. C., Schreiber, S. L. & Kruglyak, L. Genetic basis of individual differences in the response to small-molecule drugs in yeast. Nat. Genet. 39, 496-502 (2007).
39. Mülleder, M. et al. A prototrophic deletion mutant collection for yeast metabolomics and systems biology. Nat. Biotechnol. 30, 1176-1178 (2012).
40. Gerke, J., Lorenz, K. & Cohen, B. Genetic interactions between transcription factors cause natural variation in yeast. Science 323, 498-501 (2009).
41. Taylor, M. B. & Ehrenreich, I. M. Transcriptional derepression uncovers cryptic higher-order genetic interactions. PLoS Genet. 11, e1005606 (2015).
42. Forsberg, S. K. G., Bloom, J. S., Sadhu, M., Kruglyak, L. & Carlborg, Ö. Accounting for genetic interactions is necessary for accurate prediction of extreme phenotypic values of quantitative traits in yeast. bio Rxiv 059485 (Cold Spring Harbor Labs Journals, 2016).
43. Nordborg, M. & Weigel, D. Next-generation genetics in plants. Nature 456, 720-723 (2008).
44. Mackay, T. F. C. Epistasis and quantitative traits: using model organisms to study gene-gene interactions. Nat. Rev. Genet. 15, 22-33 (2014).
45. Melchinger, A. E. et al. Genetic basis of heterosis for growth-related traits in arabidopsis investigated by testcross progenies of near-isogenic lines reveals a significant role of epistasis. Genetics 177, 1827-1837 (2007).
46. Tang, J. et al. Dissection of the genetic basis of heterosis in an elite maize hybrid by QTL mapping in an immortalized F2 population. Theor. Appl. Genet. 120, 333-340 (2010).
47. Hua, J. et al. Single-locus heterotic effects and dominance by dominance interactions can adequately explain the genetic basis of heterosis in an elite rice hybrid. Proc. Natl Acad. Sci. USA 100, 2574-2579 (2003).
48. Mott, R. et al. The architecture of parent-of-origin effects in mice. Cell 156, 332-342 (2014).
49. Liti, G. et al. Population genomics of domestic and wild yeasts. Nature 458, 337-341 (2009).
50. Yang, J., Lee, S. H., Goddard, M. E. & Visscher, P. M. GCTA: a tool for genome-wide complex trait analysis. Am. J. Hum. Genet. 88, 76-82 (2011).
51. Broman, K. W. & Sen, S. A Guide to QTL Mapping with R/qtl 1-401 (Springer, 2009).
52. Lippert, C., Casale, F. P., Rakitsch, B. & Stegle, O. LIMIX: genetic analysis of multiple traits. doi:http://dx.doi.org/10.1101/003905 (2014).
53. R Core Team R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, Vienna, Austria). URL https://www.R-project.org/.
54. Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer-Verlag New York, Version 2.1.0, 2009).
55. Wickham, H. Reshaping Data with the reshape Package. J. Stat. Softw. 21, 1-20 (2007).
56. Wickham, H. Stringr: Simple, Consistent Wrappers for Common String Operations. R package version 1.0.0. http://CRAN.R-project.org/package=stringr (2015).
57. Wickham, H. The Split-Apply-Combine Strategy for Data Analysis. Journal of Statistical Software 40, 1-29 (2011).
58. Solymos, P. & Zawadzki, Z. pbapply: Adding Progress Bar to '∗apply' Functions. R package version 1.2-1. http://CRAN.R-project.org/package=pbapply (2016).