The Hidden Complexity of Mendelian Traits across Natural Yeast Populations

Cell Reports

Volumn 16, Issue 4, 2016, Pages 1106-1114

  Hou, Jing ^a   Sigwalt, Anastasie ^a   Fournier, Téo ^a   Pflieger, David ^a   Peter, Jackson ^a   de Montigny, Jacky ^a   Dunham, Maitreya J ^b   Schacherer, Joseph ^a  

^a Université de Strasbourg   (France)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CONTROLLED STUDY; FUNGUS GROWTH; FUNGUS ISOLATION; GENETIC TRAIT; GENETIC VARIABILITY; LIMIT OF QUANTITATION; MENDELIAN TRAIT; NONHUMAN; PHENOTYPE; POPULATION DISTRIBUTION; PRIORITY JOURNAL; PROGENY; SACCHAROMYCES CEREVISIAE; SPECIES DIVERSITY; GENETIC VARIATION; GENETICS; QUANTITATIVE TRAIT LOCUS;

GENETIC VARIATION; PHENOTYPE; QUANTITATIVE TRAIT LOCI; SACCHAROMYCES CEREVISIAE;

EID: 84992521988     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.06.048     Document Type: Article

References (41)

1. Anderson, J.B., Funt, J., Thompson, D.A., Prabhu, S., Socha, A., Sirjusingh, C., Dettman, J.R., Parreiras, L., Guttman, D.S., Regev, A., Kohn, L.M., Determinants of divergent adaptation and Dobzhansky-Muller interaction in experimental yeast populations. Curr. Biol. 20 (2010), 1383–1388.
2. Antonarakis, S.E., Beckmann, J.S., Mendelian disorders deserve more attention. Nat. Rev. Genet. 7 (2006), 277–282.
3. Antonarakis, S.E., Chakravarti, A., Cohen, J.C., Hardy, J., Mendelian disorders and multifactorial traits: the big divide or one for all?. Nat. Rev. Genet. 11 (2010), 380–384.
4. Auton, A., Brooks, L.D., Durbin, R.M., Garrison, E.P., Kang, H.M., Korbel, J.O., Marchini, J.L., McCarthy, S., McVean, G.A., Abecasis, G.R., 1000 Genomes Project Consortium. A global reference for human genetic variation. Nature 526 (2015), 68–74.
5. Badano, J.L., Katsanis, N., Beyond Mendel: an evolving view of human genetic disease transmission. Nat. Rev. Genet. 3 (2002), 779–789.
6. Blomen, V.A., Májek, P., Jae, L.T., Bigenzahn, J.W., Nieuwenhuis, J., Staring, J., Sacco, R., van Diemen, F.R., Olk, N., Stukalov, A., et al. Gene essentiality and synthetic lethality in haploid human cells. Science 350 (2015), 1092–1096.
7. Bloom, J.S., Ehrenreich, I.M., Loo, W.T., Lite, T.L., Kruglyak, L., Finding the sources of missing heritability in a yeast cross. Nature 494 (2013), 234–237.
8. Cao, J., Schneeberger, K., Ossowski, S., Günther, T., Bender, S., Fitz, J., Koenig, D., Lanz, C., Stegle, O., Lippert, C., et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat. Genet. 43 (2011), 956–963.
9. Cooper, D.N., Krawczak, M., Polychronakos, C., Tyler-Smith, C., Kehrer-Sawatzki, H., Where genotype is not predictive of phenotype: towards an understanding of the molecular basis of reduced penetrance in human inherited disease. Hum. Genet. 132 (2013), 1077–1130.
10. Dipple, K.M., McCabe, E.R., Modifier genes convert “simple” Mendelian disorders to complex traits. Mol. Genet. Metab. 71 (2000), 43–50.
11. Dittmar, J.C., Reid, R.J., Rothstein, R., ScreenMill: a freely available software suite for growth measurement, analysis and visualization of high-throughput screen data. BMC Bioinformatics, 11, 2010, 353.
12. Dorfman, R., Modifier gene studies to identify new therapeutic targets in cystic fibrosis. Curr. Pharm. Des. 18 (2012), 674–682.
13. Dowell, R.D., Ryan, O., Jansen, A., Cheung, D., Agarwala, S., Danford, T., Bernstein, D.A., Rolfe, P.A., Heisler, L.E., Chin, B., et al. Genotype to phenotype: a complex problem. Science, 328, 2010, 469.
14. Dunham, M.J., Badrane, H., Ferea, T., Adams, J., Brown, P.O., Rosenzweig, F., Botstein, D., Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 99 (2002), 16144–16149.
15. Ehrenreich, I.M., Bloom, J., Torabi, N., Wang, X., Jia, Y., Kruglyak, L., Genetic architecture of highly complex chemical resistance traits across four yeast strains. PLoS Genet., 8, 2012, e1002570.
16. Fay, J.C., The molecular basis of phenotypic variation in yeast. Curr. Opin. Genet. Dev. 23 (2013), 672–677.
17. Fogel, S., Welch, J.W., Tandem gene amplification mediates copper resistance in yeast. Proc. Natl. Acad. Sci. USA 79 (1982), 5342–5346.
18. Friedrich, A., Jung, P., Reisser, C., Fischer, G., Schacherer, J., Population genomics reveals chromosome-scale heterogeneous evolution in a protoploid yeast. Mol. Biol. Evol. 32 (2015), 184–192.
19. Gerstein, A.C., Ono, J., Lo, D.S., Campbell, M.L., Kuzmin, A., Otto, S.P., Too much of a good thing: the unique and repeated paths toward copper adaptation. Genetics 199 (2015), 555–571.
20. Gresham, D., Desai, M.M., Tucker, C.M., Jenq, H.T., Pai, D.A., Ward, A., DeSevo, C.G., Botstein, D., Dunham, M.J., The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet., 4, 2008, e1000303.
21. Hamilton, B.A., Yu, B.D., Modifier genes and the plasticity of genetic networks in mice. PLoS Genet., 8, 2012, e1002644.
22. Hart, T., Chandrashekhar, M., Aregger, M., Steinhart, Z., Brown, K.R., MacLeod, G., Mis, M., Zimmermann, M., Fradet-Turcotte, A., Sun, S., et al. High-resolution CRISPR screens reveal fitness genes and genotype-specific cancer liabilities. Cell 163 (2015), 1515–1526.
23. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., 1000 Genome Project Data Processing Subgroup. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25 (2009), 2078–2079.
24. Liti, G., Carter, D.M., Moses, A.M., Warringer, J., Parts, L., James, S.A., Davey, R.P., Roberts, I.N., Burt, A., Koufopanou, V., et al. Population genomics of domestic and wild yeasts. Nature 458 (2009), 337–341.
25. Mackay, T.F., Stone, E.A., Ayroles, J.F., The genetics of quantitative traits: challenges and prospects. Nat. Rev. Genet. 10 (2009), 565–577.
26. McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., DePristo, M.A., The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20 (2010), 1297–1303.
27. Moye-Rowley, W.S., Transcriptional control of multidrug resistance in the yeast Saccharomyces. Prog. Nucleic Acid Res. Mol. Biol. 73 (2003), 251–279.
28. Mukherjee, V., Steensels, J., Lievens, B., Van de Voorde, I., Verplaetse, A., Aerts, G., Willems, K.A., Thevelein, J.M., Verstrepen, K.J., Ruyters, S., Phenotypic evaluation of natural and industrial Saccharomyces yeasts for different traits desirable in industrial bioethanol production. Appl. Microbiol. Biotechnol. 98 (2014), 9483–9498.
29. Nadeau, J.H., Modifier genes in mice and humans. Nat. Rev. Genet. 2 (2001), 165–174.
30. Paaby, A.B., White, A.G., Riccardi, D.D., Gunsalus, K.C., Piano, F., Rockman, M.V., Wild worm embryogenesis harbors ubiquitous polygenic modifier variation. eLife, 4, 2015, 09178.
31. Reisser, C., Dick, C., Kruglyak, L., Botstein, D., Schacherer, J., Hess, D., Genetic basis of ammonium toxicity resistance in a sake strain of yeast: a Mendelian case. G3 (Bethesda) 3 (2013), 733–740.
32. Ruiz, A., Ariño, J., Function and regulation of the Saccharomyces cerevisiae ENA sodium ATPase system. Eukaryot. Cell 6 (2007), 2175–2183.
33. Schacherer, J., Shapiro, J.A., Ruderfer, D.M., Kruglyak, L., Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458 (2009), 342–345.
34. Sing, T., Sander, O., Beerenwinkel, N., Lengauer, T., ROCR: visualizing classifier performance in R. Bioinformatics 21 (2005), 3940–3941.
35. Steinmetz, L.M., Sinha, H., Richards, D.R., Spiegelman, J.I., Oefner, P.J., McCusker, J.H., Davis, R.W., Dissecting the architecture of a quantitative trait locus in yeast. Nature 416 (2002), 326–330.
36. Strope, P.K., Skelly, D.A., Kozmin, S.G., Mahadevan, G., Stone, E.A., Magwene, P.M., Dietrich, F.S., McCusker, J.H., The 100-genomes strains, an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen. Genome Res. 25 (2015), 762–774.
37. Thein, S.L., Genetic modifiers of sickle cell disease. Hemoglobin 35 (2011), 589–606.
38. Treusch, S., Albert, F.W., Bloom, J.S., Kotenko, I.E., Kruglyak, L., Genetic mapping of MAPK-mediated complex traits Across S. cerevisiae. PLoS Genet., 11, 2015, e1004913.
39. Vu, V., Verster, A.J., Schertzberg, M., Chuluunbaatar, T., Spensley, M., Pajkic, D., Hart, G.T., Moffat, J., Fraser, A.G., Natural variation in gene expression modulates the severity of mutant phenotypes. Cell 162 (2015), 391–402.
40. Wagih, O., Parts, L., gitter: a robust and accurate method for quantification of colony sizes from plate images. G3 (Bethesda) 4 (2014), 547–552.
41. Wang, T., Birsoy, K., Hughes, N.W., Krupczak, K.M., Post, Y., Wei, J.J., Lander, E.S., Sabatini, D.M., Identification and characterization of essential genes in the human genome. Science 350 (2015), 1096–1101.