Gene-Environment Interactions in Stress Response Contribute Additively to a Genotype-Environment Interaction

PLoS Genetics

Volumn 12, Issue 7, 2016, Pages

  Matsui, Takeshi ^a   Ehrenreich, Ian M ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; GLUCOSE; FUNGAL PROTEIN;

ALLELE; ARTICLE; CARBON SOURCE; CONTROLLED STUDY; DNA POLYMORPHISM; ENVIRONMENTAL STRESS; FUNGAL STRAIN; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; GENE LOCUS; GENETIC VARIATION; GENOTYPE ENVIRONMENT INTERACTION; MOLECULAR CLONING; MOLECULAR GENETICS; NONHUMAN; PHENOTYPE; BIOLOGICAL MODEL; CHEMISTRY; CHROMOSOMAL MAPPING; CROSS BREEDING; FUNGAL GENE; GENETIC ENGINEERING; GENETICS; GENOMICS; GENOTYPE; HAPLOIDY; METABOLISM; PHYSIOLOGICAL STRESS; POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; TEMPERATURE;

ALLELES; CHROMOSOME MAPPING; CROSSES, GENETIC; ETHANOL; FUNGAL PROTEINS; GENE-ENVIRONMENT INTERACTION; GENES, FUNGAL; GENETIC ENGINEERING; GENETIC LOCI; GENOMICS; GENOTYPE; GLUCOSE; HAPLOIDY; MODELS, GENETIC; PHENOTYPE; POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; STRESS, PHYSIOLOGICAL; TEMPERATURE;

EID: 84982840714     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006158     Document Type: Article

References (49)

1. Falconer DS, Mackay TF, (1996) Introduction to quantitative genetics (4th edition). Harlow, England: Pearson Education Limited.
2. Lynch M, Walsh B, (1998) Genetics and analysis of quantitative traits. Sunderland, Massachusetts: Sinauer Associates, Inc.
3. Mackay TF, Stone EA, Ayroles JF, (2009) The genetics of quantitative traits: challenges and prospects. Nat Rev Genet10: 565–577. doi: 10.1038/nrg261219584810
4. Baye TM, Abebe T, Wilke RA, (2011) Genotype-environment interactions and their translational implications. Per Med8: 59–70. 21660115
5. Rauw WM, Gomez-Raya L, (2015) Genotype by environment interaction and breeding for robustness in livestock. Front Genet6: 310. doi: 10.3389/fgene.2015.0031026539207
6. Zeng ZB, (2005) QTL mapping and the genetic basis of adaptation: recent developments. Genetica123: 25–37. 15881678
7. Bhatia A, Yadav A, Zhu C, Gagneur J, Radhakrishnan A, et al. (2014) Yeast growth plasticity is regulated by environment-specific multi-QTL interactions. G34: 769–777. doi: 10.1534/g3.113.00914224474169
8. Gerke J, Lorenz K, Ramnarine S, Cohen B, (2010) Gene-environment interactions at nucleotide resolution. PLoS Genet6: e1001144. doi: 10.1371/journal.pgen.100114420941394
9. Lee JT, Taylor MB, Shen A, Ehrenreich IM, (2016) Multi-locus genotypes underlying temperature sensitivity in a mutationally induced trait. PLoS Genet12: e1005929. doi: 10.1371/journal.pgen.100592926990313
10. Liti G, Carter DM, Moses AM, Warringer J, Parts L, et al. (2009) Population genomics of domestic and wild yeasts. Nature458: 337–341. doi: 10.1038/nature0774319212322
11. Kvitek DJ, Will JL, Gasch AP, (2008) Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolates. PLoS Genet4: e1000223. doi: 10.1371/journal.pgen.100022318927628
12. Broach JR, (2012) Nutritional control of growth and development in yeast. Genetics192: 73–105. doi: 10.1534/genetics.111.13573122964838
13. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, et al. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell11: 4241–4257. 11102521
14. Steinmetz LM, Sinha H, Richards DR, Spiegelman JI, Oefner PJ, et al. (2002) Dissecting the architecture of a quantitative trait locus in yeast. Nature416: 326–330. 11907579
15. Yang Y, Foulquie-Moreno MR, Clement L, Erdei E, Tanghe A, et al. (2013) QTL analysis of high thermotolerance with superior and downgraded parental yeast strains reveals new minor QTLs and converges on novel causative alleles involved in RNA processing. PLoS Genet9: e1003693. doi: 10.1371/journal.pgen.100369323966873
16. Sinha H, David L, Pascon RC, Clauder-Munster S, Krishnakumar S, et al. (2008) Sequential elimination of major-effect contributors identifies additional quantitative trait loci conditioning high-temperature growth in yeast. Genetics180: 1661–1670. doi: 10.1534/genetics.108.09293218780730
17. Sinha H, Nicholson BP, Steinmetz LM, McCusker JH, (2006) Complex genetic interactions in a quantitative trait locus. PLoS Genet2: e13. 16462944
18. Gagneur J, Stegle O, Zhu C, Jakob P, Tekkedil MM, et al. (2013) Genotype-environment interactions reveal causal pathways that mediate genetic effects on phenotype. PLoS Genet9: e1003803. doi: 10.1371/journal.pgen.100380324068968
19. McCusker JH, Clemons KV, Stevens DA, Davis RW, (1994) Saccharomyces cerevisiae virulence phenotype as determined with CD-1 mice is associated with the ability to grow at 42 degrees C and form pseudohyphae. Infect Immun62: 5447–5455. 7960125
20. McCusker JH, Clemons KV, Stevens DA, Davis RW, (1994) Genetic characterization of pathogenic Saccharomyces cerevisiae isolates. Genetics136: 1261–1269. 8013903
21. Mitchell SF, Jain S, She M, Parker R, (2013) Global analysis of yeast mRNPs. Nat Struct Mol Biol20: 127–133. doi: 10.1038/nsmb.246823222640
22. Cherry JM, Hong EL, Amundsen C, Balakrishnan R, Binkley G, et al. (2012) Saccharomyces genome database: The genomics resource of budding yeast. Nucleic acids research40: D700–705. doi: 10.1093/nar/gkr102922110037
23. Wout PK, Sattlegger E, Sullivan SM, Maddock JR, (2009) Saccharomyces cerevisiae Rbg1 protein and its binding partner Gir2 interact on Polyribosomes with Gcn1. Eukaryot Cell8: 1061–1071. doi: 10.1128/EC.00356-0819448108
24. Buchan JR, Muhlrad D, Parker R, (2008) P bodies promote stress granule assembly in Saccharomyces cerevisiae. J Cell Biol183: 441–455. doi: 10.1083/jcb.20080704318981231
25. Buchan JR, Parker R, (2009) Eukaryotic stress granules: the ins and outs of translation. Mol Cell36: 932–941. doi: 10.1016/j.molcel.2009.11.02020064460
26. Decker CJ, Parker R, (2012) P-bodies and stress granules: possible roles in the control of translation and mRNA degradation. Cold Spring Harb Perspect Biol4: a012286. doi: 10.1101/cshperspect.a01228622763747
27. Li SC, Kane PM, (2009) The yeast lysosome-like vacuole: endpoint and crossroads. Biochim Biophys Acta1793: 650–663. doi: 10.1016/j.bbamcr.2008.08.00318786576
28. Voordeckers K, Kominek J, Das A, Espinosa-Cantu A, De Maeyer D, et al. (2015) Adaptation to high ethanol reveals complex evolutionary pathways. PLoS Genet11: e1005635. doi: 10.1371/journal.pgen.100563526545090
29. Duitama J, Sanchez-Rodriguez A, Goovaerts A, Pulido-Tamayo S, Hubmann G, et al. (2014) Improved linkage analysis of Quantitative Trait Loci using bulk segregants unveils a novel determinant of high ethanol tolerance in yeast. BMC Genomics15: 207. doi: 10.1186/1471-2164-15-20724640961
30. Gibson G, (2009) Decanalization and the origin of complex disease. Nat Rev Genet10: 134–140. doi: 10.1038/nrg250219119265
31. Bloom JS, Ehrenreich IM, Loo WT, Lite TL, Kruglyak L, (2013) Finding the sources of missing heritability in a yeast cross. Nature494: 234–237. doi: 10.1038/nature1186723376951
32. Bloom JS, Kotenko I, Sadhu MJ, Treusch S, Albert FW, et al. (2015) Genetic interactions contribute less than additive effects to quantitative trait variation in yeast. Nat Commun6: 8712. doi: 10.1038/ncomms971226537231
33. Linder RA, Seidl F, Ha K, Ehrenreich IM, (2016) The complex genetic and molecular basis of a model quantitative trait. Mol Biol Cell27: 209–218. doi: 10.1091/mbc.E15-06-040826510497
34. Omholt SW, Plahte E, Oyehaug L, Xiang K, (2000) Gene regulatory networks generating the phenomena of additivity, dominance and epistasis. Genetics155: 969–980. 10835414
35. Gjuvsland AB, Hayes BJ, Omholt SW, Carlborg O, (2007) Statistical epistasis is a generic feature of gene regulatory networks. Genetics175: 411–420. 17028346
36. Taylor MB, Ehrenreich IM, (2014) Genetic interactions involving five or more genes contribute to a complex trait in yeast. PLoS Genet10: e1004324. doi: 10.1371/journal.pgen.100432424784154
37. Taylor MB, Ehrenreich IM, (2015) Higher-order genetic interactions and their contribution to complex traits. Trends Genet31: 34–40. doi: 10.1016/j.tig.2014.09.00125284288
38. Taylor MB, Ehrenreich IM, (2015) Transcriptional derepression uncovers cryptic higher-order genetic interactions. PLoS Genet11: e1005606. doi: 10.1371/journal.pgen.100560626484664
39. Taylor MB, Phan J, Lee JT, McCadden M, Ehrenreich IM, (2016) Diverse genetic architectures lead to the same cryptic phenotype in a yeast cross. Nature Communications7: 11669. doi: 10.1038/ncomms1166927248513
40. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, et al. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science294: 2364–2368. 11743205
41. Sherman F, Guthrie C, Fink GR, (1991) Guide to yeast genetics and molecular biology. In: Methods in Enzymology. San Diego, California: Elsevier Academic Press. pp. 3–21.
42. Ehrenreich IM, Torabi N, Jia Y, Kent J, Martis S, et al. (2010) Dissection of genetically complex traits with extremely large pools of yeast segregants. Nature464: 1039–1042. doi: 10.1038/nature0892320393561
43. Matsui T, Linder R, Phan J, Seidl F, Ehrenreich IM, (2015) Regulatory rewiring in a cross causes extensive genetic heterogeneity. Genetics201: 769–777. doi: 10.1534/genetics.115.18066126232408
44. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics25: 1754–1760. doi: 10.1093/bioinformatics/btp32419451168
45. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics25: 2078–2079. doi: 10.1093/bioinformatics/btp35219505943
46. Schneider CA, Rasband WS, Eliceiri KW, (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods9: 671–675. 22930834
47. Erdeniz N, Mortensen UH, Rothstein R, (1997) Cloning-free PCR-based allele replacement methods. Genome Res7: 1174–1183. 9414323
48. Strope PK, Skelly DA, Kozmin SG, Mahadevan G, Stone EA, et al. (2015) The 100-genomes strains, an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen. Genome Res25: 762–774. doi: 10.1101/gr.185538.11425840857
49. Mitchell A, Chang HY, Daugherty L, Fraser M, Hunter S, et al. (2015) The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res43: D213–221. doi: 10.1093/nar/gku124325428371