Comprehensive survey of condition-specific reproductive isolation reveals genetic incompatibility in yeast

Nature Communications

Volumn 6, Issue , 2015, Pages

  Hou, Jing ^a   Friedrich, Anne ^a   Gounot, Jean Sebastien ^a   Schacherer, Joseph ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSFER RNA; BEM2 PROTEIN, S CEREVISIAE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; STOP CODON;

EPISTASIS; FERTILITY; REPRODUCTIVE ISOLATION; YEAST;

ADAPTATION; ARTICLE; BULKED SEGREGANT ANALYSIS; CHROMOSOME; CONTROLLED STUDY; DNA SEQUENCE; ENVIRONMENTAL FACTOR; EPISTASIS; FUNGAL GENE; FUNGUS GROWTH; GENE FREQUENCY; GENE IDENTIFICATION; GENE LOCUS; GENETIC INCOMPATIBILITY; GENETIC SELECTION; GENOTYPE ENVIRONMENT INTERACTION; MITOCHONDRIAL GENE; NATURAL POPULATION; NONHUMAN; NONSENSE MUTATION; PHENOTYPE; PROGENY; REPRODUCTIVE FITNESS; REPRODUCTIVE ISOLATION; SACCHAROMYCES CEREVISIAE; STOP CODON; EVOLUTION; GENETICS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SUPPRESSOR GENE;

SACCHAROMYCES CEREVISIAE;

BIOLOGICAL EVOLUTION; CODON, NONSENSE; GENE-ENVIRONMENT INTERACTION; GENES, SUPPRESSOR; GENETIC FITNESS; GTPASE-ACTIVATING PROTEINS; REPRODUCTIVE ISOLATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRESS, PHYSIOLOGICAL;

EID: 84930227166     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8214     Document Type: Article

References (52)

1. Coyne, J. A. & Orr, H. A. Speciation, xiii, 545, 2 p. of plates (Sinauer Associates, 2004).
2. Presgraves, D. C. The molecular evolutionary basis of species formation. Nat. Rev. Genet. 11, 175-180 (2010).
3. Chen, C. et al. A two-locus interaction causes interspecific hybrid weakness in rice. Nat. Commun. 5, 3357 (2014).
4. Maheshwari, S. & Barbash, D. A. The genetics of hybrid incompatibilities. Annu. Rev. Genet. 45, 331-355 (2011).
5. Ouyang, Y. & Zhang, Q. Understanding reproductive isolation based on the rice model. Annu. Rev. Plant Biol. 64, 111-135 (2013).
6. Greig, D. Reproductive isolation in Saccharomyces. Heredity (Edinb) 102, 39-44 (2009).
7. Chou, J. Y. & Leu, J. Y. Speciation through cytonuclear incompatibility: insights from yeast and implications for higher eukaryotes. Bioessays 32, 401-411 (2010).
8. Zanders, S. E. et al. Genome rearrangements and pervasive meiotic drive cause hybrid infertility in fission yeast. Elife 3, e02630 (2014).
9. Bomblies, K. & Weigel, D. Arabidopsis: a model genus for speciation. Curr. Opin. Genet. Dev. 17, 500-504 (2007).
10. Seidel, H. S., Rockman, M. V. & Kruglyak, L. Widespread genetic incompatibility in C. elegans maintained by balancing selection. Science 319, 589-594 (2008).
11. Paliwal, S., Fiumera, A. C. & Fiumera, H. L. Mitochondrial-nuclear epistasis contributes to phenotypic variation and coadaptation in natural isolates of Saccharomyces cerevisiae. Genetics 198, 1251-1265 (2014).
12. Bikard, D. et al. Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science 323, 623-626 (2009).
13. Corbett-Detig, R. B., Zhou, J., Clark, A. G., Hartl, D. L. & Ayroles, J. F. Genetic incompatibilities are widespread within species. Nature 504, 135-137 (2013).
14. Charron, G., Leducq, J. B. & Landry, C. R. Chromosomal variation segregates within incipient species and correlates with reproductive isolation. Mol. Ecol. 23, 4362-4372 (2014).
15. Hou, J., Friedrich, A., de Montigny, J. & Schacherer, J. Chromosomal rearrangements as a major mechanism in the onset of reproductive isolation in Saccharomyces cerevisiae. Curr. Biol. 24, 1153-1159 (2014).
16. Chae, E. et al. Species-wide genetic incompatibility analysis identifies immune genes as hot spots of deleterious epistasis. Cell 159, 1341-1351 (2014).
17. Seidel, H. S. et al. A novel sperm-delivered toxin causes late-stage embryo lethality and transmission ratio distortion in C elegans. PLoS Biol. 9, e1001115 (2011).
18. Alcazar, R., Garcia, A. V., Parker, J. E. & Reymond, M. Incremental steps toward incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic acid pathway activation. Proc. Natl Acad. Sci. USA 106, 334-339 (2009).
19. Bomblies, K. & Weigel, D. Hybrid necrosis: autoimmunity as a potential geneflow barrier in plant species. Nat. Rev. Genet. 8, 382-393 (2007).
20. Alcazar, R. & Parker, J. E. The impact of temperature on balancing immune responsiveness and growth in Arabidopsis. Trends Plant Sci. 16, 666-675 (2011).
21. Schacherer, J., Shapiro, J. A., Ruderfer, D. M. & Kruglyak, L. Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458, 342-345 (2009).
22. Adams, A. E. & Botstein, D. Dominant suppressors of yeast actin mutations that are reciprocally suppressed. Genetics 121, 675-683 (1989).
23. Broach, J. R., Friedman, L. & Sherman, F. Correspondence of yeast UAA suppressors to cloned tRNASerUCA genes. J. Mol. Biol. 150, 375-387 (1981).
24. Gesteland, R. F. et al. Yeast suppressors of UAA and UAG nonsense codons work efficiently in vitro via tRNA. Cell 7, 381-390 (1976).
25. Novick, P., Osmond, B. C. & Botstein, D. Suppressors of yeast actin mutations. Genetics 121, 659-674 (1989).
26. Ono, B. I., Tanaka, M., Kominami, M., Ishino, Y. & Shinoda, S. Recessive UAA suppressors of the yeast Saccharomyces cerevisiae. Genetics 102, 653-664 (1982).
27. McCusker, J. H., Clemons, K. V., Stevens, D. A. & Davis, R. W. Genetic characterization of pathogenic Saccharomyces cerevisiae isolates. Genetics 136, 1261-1269 (1994).
28. Merz, S. & Westermann, B. Genome-wide deletion mutant analysis reveals genes required for respiratory growth, mitochondrial genome maintenance and mitochondrial protein synthesis in Saccharomyces cerevisiae. Genome Biol. 10, R95 (2009).
29. Skelly, D. A. et al. Integrative phenomics reveals insight into the structure of phenotypic diversity in budding yeast. Genome Res. 23, 1496-1504 (2013).
30. Strope, P. K. et al. 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, 762-774 (2015).
31. Fischer, G., James, S. A., Roberts, I. N., Oliver, S. G. & Louis, E. J. Chromosomal evolution in Saccharomyces. Nature 405, 451-454 (2000).
32. Hunter, N., Chambers, S. R., Louis, E. J. & Borts, R. H. The mismatch repair system contributes to meiotic sterility in an interspecific yeast hybrid. EMBO J. 15, 1726-1733 (1996).
33. Delneri, D. et al. Engineering evolution to study speciation in yeasts. Nature 422, 68-72 (2003).
34. Chou, J. Y., Hung, Y. S., Lin, K. H., Lee, H. Y. & Leu, J. Y. Multiple molecular mechanisms cause reproductive isolation between three yeast species. PLoS Biol. 8, e1000432 (2010).
35. Lee, H. Y. et al. Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135, 1065-1073 (2008).
36. Li, C., Wang, Z. & Zhang, J. Toward genome-wide identification of Bateson-Dobzhansky-Muller incompatibilities in yeast: a simulation study. Genome Biol. Evol. 5, 1261-1272 (2013).
37. Greig, D. A screen for recessive speciation genes expressed in the gametes of F1 hybrid yeast. PLoS Genet. 3, e21 (2007).
38. Greig, D., Borts, R. H., Louis, E. J. & Travisano, M. Epistasis and hybrid sterility in Saccharomyces. Proc. Biol. Sci. 269, 1167-1171 (2002).
39. Demogines, A., Wong, A., Aquadro, C. & Alani, E. Incompatibilities involving yeast mismatch repair genes: a role for genetic modifiers and implications for disease penetrance and variation in genomic mutation rates. PLoS Genet. 4, e1000103 (2008).
40. Heck, J. A. et al. Negative epistasis between natural variants of the Saccharomyces cerevisiae MLH1 and PMS1 genes results in a defect in mismatch repair. Proc. Natl Acad. Sci. USA 103, 3256-3261 (2006).
41. Vandenbosch, D. et al. Genomewide screening for genes involved in biofilm formation and miconazole susceptibility in Saccharomyces cerevisiae. FEMS Yeast Res. 13, 720-730 (2013).
42. Shorter, J. & Lindquist, S. Prions as adaptive conduits of memory and inheritance. Nat. Rev. Genet. 6, 435-450 (2005).
43. Torabi, N. & Kruglyak, L. Genetic basis of hidden phenotypic variation revealed by increased translational readthrough in yeast. PLoS Genet. 8, e1002546 (2012).
44. Yu, W. & Spreitzer, R. J. Chloroplast heteroplasmicity is stabilized by an ambersuppressor tryptophan tRNA(CUA). Proc. Natl Acad. Sci. USA 89, 3904-3907 (1992).
45. Halfmann, R. et al. Prions are a common mechanism for phenotypic inheritance in wild yeasts. Nature 482, 363-368 (2012).
46. 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, 184-192 (2015).
47. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
48. 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, e1004913 (2015).
49. Jung, P. P., Christian, N., Kay, D. P., Skupin, A. & Linster, C. L. Protocols and programs for high-throughput growth and aging phenotyping in yeast. PLoS One 10, e0119807.
50. Wagih, O. & Parts, L. gitter: a robust and accurate method for quantification of colony sizes from plate images. G3 (Bethesda) 4, 547-552 (2014).
51. Robinson, M. D., Grigull, J., Mohammad, N. & Hughes, T. R. FunSpec: a webbased cluster interpreter for yeast. BMC Bioinformatics 3, 35 (2002).
52. Luo, R. et al. SOAPdenovo2: an empirically improved memory-efficient shortread de novo assembler. Gigascience 1, 18 (2012).