Genes with a combination of over-dominant and epistatic effects underlie heterosis in growth of Saccharomyces cerevisiae at high temperature

Frontiers in Genetics

Volumn 7, Issue MAY, 2016, Pages

  Shapira, Rachel ^a,b   David, Lior ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Epistasis; Genetic interaction; Hybrid vigor; Over dominance; QTL; Quantitative traits; Yeast

Indexed keywords

ALLELE; CLINICAL ARTICLE; DOMINANT GENE; EPISTASIS; FOOD INDUSTRY; FUNGAL CELL CULTURE; GENE INTERACTION; HETEROSIS; HETEROZYGOSITY; HIGH TEMPERATURE; HOMOZYGOSITY; HUMAN; MODEL; QUANTITATIVE TRAIT; SACCHAROMYCES CEREVISIAE;

EID: 84975261070     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2016.00072     Document Type: Article

References (53)

1. Altshuler, D., Daly, M. J., and Lander, E. S. (2008). Genetic mapping in human disease. Science 322, 881-888. doi: 10.1126/science.1156409
2. Baranwal, V. K., Mikkilineni, V., Zehr, U. B., Tyagi, A. K., and Kapoor, S. (2012). Heterosis: emerging ideas about hybrid vigour. J. Exp. Bot. 63, 6309-6314. doi: 10.1093/jxb/ers291
3. Ben-Israel, I., Kilian, B., Nida, H., and Fridman, E. (2012). Heterotic trait locus (HTL) mapping identifies intra-locus interactions that underlie reproductive hybrid vigor in Sorghum bicolor. PLoS ONE 7:e38993. doi: 10.1371/journal.pone.0038993
4. Birchler, J. A., Yao, H., Chudalayandi, S., Vaiman, D., and Veitia, R. A. (2010). Heterosis. Plant Cell 22, 2105-2112. doi: 10.1105/tpc.110.076133
5. Bruce, A. B. (1910). The mendelian theory of heredity and the augmentation of vigor. Science 32, 627-628. doi: 10.1126/science.32.827.627-a
6. Charlesworth, D., and Willis, J. H. (2009). The genetics of inbreeding depression. Nat. Rev. Genet. 10, 783-796. doi: 10.1038/nrg2664
7. Chen, Z. J. (2010). Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci. 15, 57-71. doi: 10.1016/j.tplants.2009.12.003
8. Comstock, R. E., and Robinson, H. F. (1949). The components of genetic variance in populations of biparental progenies and their use in estimating the average degree of dominance. Biometrics 4, 254-266. doi: 10.2307/3001412
9. Comstock, R. E., Robinson, H. F., and Harvey, P. H. (1949). A breeding procedure designed to make maximum use of both general and specific combining ability. Agron. J. 41, 360-367. doi: 10.2134/agronj1949.00021962004100080006x
10. Crow, J. F. (1948). Alternative hypotheses of hybrid vigor. Genetics 33, 477-487
11. Dallabona, C., Marsano, R. M., Arzuffi, P., Ghezzi, D., Mancini, P., Zeviani, M., et al. (2010). Sym1, the yeast ortholog of the MPV17 human disease protein, is a stress-induced bioenergetic and morphogenetic mitochondrial modulator. Hum. Mol. Genet. 19, 1098-1107. doi: 10.1093/hmg/ddp581
12. de Visser, J. A., Cooper, T. F., and Elena, S. F. (2011). The causes of epistasis. Proc. Biol. Sci. 278, 3617-3624. doi: 10.1098/rspb.2011.1537
13. Deutschbauer, A. M., and Davis, R. W. (2005). Quantitative trait loci mapped to single-nucleotide resolution in yeast. Nat. Genet. 37, 1333-1340. doi: 10.1038/ng1674
14. East, E. M. (1908). Inbreeding in corn. Rep. Conn. Agric. Exp. Stn. 1907, 419-428
15. East, E. M. (1936). Heterosis. Genetics 21, 375-397
16. Ehrenreich, I. M., Torabi, N., Jia, Y., Kent, J., Martis, S., Shapiro, J. A., et al. (2010). Dissection of genetically complex traits with extremely large pools of yeast segregants. Nature 464, 1039-1042. doi: 10.1038/nature08923
17. Ellis, T. P., Helfenbein, K. G., Tzagoloff, A., and Dieckmann, C. L. (2004). Aep3p stabilizes the mitochondrial bicistronic mRNA encoding subunits 6 and 8 of the H+-translocating ATP synthase of Saccharomyces cerevisiae. J. Biol. Chem. 279, 15728-15733. doi: 10.1074/jbc.M314162200
18. Falk, R. (1961). Are induced mutations in Drosophila overdominant? II. Experimental results. Genetics 46, 737-757
19. Flint, J., and Mackay, T. F. (2009). Genetic architecture of quantitative traits in mice, flies, and humans. Genome Res. 19, 723-733. doi: 10.1101/gr.086660.108
20. Frazer, K. A., Murray, S. S., Schork, N. J., and Topol, E. J. (2009). Human genetic variation and its contribution to complex traits. Nat. Rev. Genet. 10, 241-251. doi: 10.1038/nrg2554
21. Gietz, R. D., and Woods, R. A. (2002). Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350, 87-96. doi: 10.1016/S0076-6879(02)50957-5
22. He, X. H., Qin, H., Hu, Z., Zhang, T., and Zhang, Y. M. (2011). Mapping of epistatic quantitative trait loci in four-way crosses. Theor. Appl. Genet. 122, 33-48. doi: 10.1007/s00122-010-1420-8
23. Hedgecock, D., Lin, J. Z., DeCola, S., Haudenschild, C. D., Meyer, E., Manahan, D. T., et al. (2007). Transcriptomic analysis of growth heterosis in larval Pacific oysters (Crassostrea gigas). Proc. Natl. Acad. Sci. U.S.A. 104, 2313-2318. doi: 10.1073/pnas.0610880104
24. Hua, J., Xing, Y., Wu, W., Xu, C., Sun, X., Yu, S., et al. (2003). 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. U.S.A. 100, 2574-2579. doi: 10.1073/pnas.0437907100
25. Kane, S. M., and Roth, R. (1974). Carbohydrate metabolism during ascospore development in yeast. J. Bacteriol. 118, 8-14
26. Krieger, U., Lippman, Z. B., and Zamir, D. (2010). The flowering gene single flower truss drives heterosis for yield in tomato. Nat. Genet. 42, 459-463. doi: 10.1038/ng.550
27. Larièpe, A., Mangin, B., Jasson, S., Combes, V., Dumas, F., Jamin, P., et al. (2012). The genetic basis of heterosis: multiparental quantitative trait loci mapping reveals contrasted levels of apparent overdominance among traits of agronomical interest in maize (Zea mays L.). Genetics 190, 795-811. doi: 10.1534/genetics.111.133447
28. Lee, C., Tibbetts, A. S., Kramer, G., and Appling, D. R. (2009). Yeast AEP3p is an accessory factor in initiation of mitochondrial translation. J. Biol. Chem. 284, 34116-34125. doi: 10.1074/jbc.M109.055350
29. Li, W., Zhu, H., Challa, G. S., and Zhang, Z. (2013). A non-additive interaction in a single locus causes a very short root phenotype in wheat. Theor. Appl. Genet. 126, 1189-1200. doi: 10.1007/s00122-013-2046-4
30. Li, Y., Zhang, X., Ma, C., Shen, J., Chen, Q., Wang, T., et al. (2012). QTL and epistatic analyses of heterosis for seed yield and three yield component traits using molecular markers in rapeseed (Brassica napus L.). Genetika 48, 1171-1178. doi: 10.1134/s1022795412050146
31. Lippman, Z. B., and Zamir, D. (2007). Heterosis: revisiting the magic. Trends Genet. 23, 60-66. doi: 10.1016/j.tig.2006.12.006
32. Liti, G., Carter, D. M., Moses, A. M., Warringer, J., Parts, L., James, S. A., et al. (2009). Population genomics of domestic and wild yeasts. Nature 458, 337-341. doi: 10.1038/nature07743
33. Mackay, T. F., Stone, E. A., and Ayroles, J. F. (2009). The genetics of quantitative traits: challenges and prospects. Nat. Rev. Genet. 10, 565-577. doi: 10.1038/nrg2612
34. Mancera, E., Bourgon, R., Huber, W., and Steinmetz, L. M. (2011). Genome-wide survey of post-meiotic segregation during yeast recombination. Genome Biol. 12, R36. doi: 10.1186/gb-2011-12-4-r36
35. Mauricio, R. (2001). Mapping quantitative trait loci in plants: uses and caveats for evolutionary biology. Nat. Rev. Genet. 2, 370-381. doi: 10.1038/35072085
36. Melchinger, A. E., Utz, H. F., Piepho, H. P., Zeng, Z. B., and Schön, C. C. (2007). The role of epistasis in the manifestation of heterosis: a systems-oriented approach. Genetics 177, 1815-1825. doi: 10.1534/genetics.107.077537
37. Melchinger, A. E., Utz, H. F., and Schön, C. C. (2008). Genetic expectations of quantitative trait loci main and interaction effects obtained with the triple testcross design and their relevance for the analysis of heterosis. Genetics 178, 2265-2274. doi: 10.1534/genetics.107.084871
38. Muller, H. J., and Falk, R. (1961). Are induced mutations in Drosophila overdominant? I. Experimental design. Genetics 46, 727-735
39. Parts, L., Cubillos, F. A., Warringer, J., Jain, K., Salinas, F., Bumpstead, S. J., et al. (2011). Revealing the genetic structure of a trait by sequencing a population under selection. Genome Res. 21, 1131-1138. doi: 10.1101/gr.116731.110
40. Saeed, A., Shahid, M. Q., Anjum, S. A., Khan, A. A., Shakeel, A., Saleem, M. F., et al. (2011). Genetic analysis of NaCl tolerance in tomato. Genet. Mol. Res. 10, 1754-1776. doi: 10.4238/vol10-3gmr1198
41. Schnable, P. S., and Springer, N. M. (2013). Progress toward understanding heterosis in crop plants. Annu. Rev. Plant Biol. 64, 71-88. doi: 10.1146/annurev-arplant-042110-103827
42. Shapira, R., Levy, T., Shaked, S., Fridman, E., and David, L. (2014). Extensive heterosis in growth of yeast hybrids is explained by a combination of genetic models. Heredity 113, 316-326. doi: 10.1038/hdy.2014.33
43. Shull, G. H. (1908). The composition of field of maize. Am. Breed. Assn. Rep. 4, 296-301. doi: 10.1093/jhered/os-4.1.296
44. Shull, G. H. (1911). The genotypes of maize. Am. Nat. 45, 234-252. doi: 10.1086/279207
45. Solberg Woods, L. C. (2014). QTL mapping in outbred populations: successes and challenges. Physiol. Genomics 46, 81-90. doi: 10.1152/physiolgenomics.00127.2013
46. Storici, F., Durham, C. L., Gordenin, D. A., and Resnick, M. A. (2003). Chromosomal site-specific double-strand breaks are efficiently targeted for repair by oligonucleotides in yeast. Proc. Natl. Acad. Sci. U.S.A. 100, 14994-14999. doi: 10.1073/pnas.2036296100
47. Vorachek-Warren, M. K., and McCusker, J. H. (2004). DsdA (D-serine deaminase): a new heterologous MX cassette for gene disruption and selection in Saccharomyces cerevisiae. Yeast 21, 163-171. doi: 10.1002/yea.1074
48. Wall, J. D., and Pritchard, J. K. (2003). Haplotype blocks and linkage disequilibrium in the human genome. Nat. Rev. Genet. 4, 587-597. doi: 10.1038/nrg1123
49. Wallace, B. (1957). The effect of heterozygosity for new mutations on viability in drosophila: a preliminary report. Proc. Natl. Acad. Sci. U.S.A. 43, 404-407. doi: 10.1073/pnas.43.5.404
50. Wilkening, S., Tekkedil, M. M., Lin, G., Fritsch, E. S., Wei, W., Gagneur, J., et al. (2013). Genotyping 1000 yeast strains by next-generation sequencing. BMC Genomics 14:90. doi: 10.1186/1471-2164-14-90
51. Winzeler, E. A., Richards, D. R., Conway, A. R., Goldstein, A. L., Kalman, S., McCullough, M. J., et al. (1998). Direct allelic variation scanning of the yeast genome. Science 281, 1194-1197. doi: 10.1126/science.281.5380.1194
52. Young, E. T., Dombek, K. M., Tachibana, C., and Ideker, T. (2003). Multiple pathways are co-regulated by the protein kinase Snf1 and the transcription factors Adr1 and Cat8. J. Biol. Chem. 278, 26146-26158. doi: 10.1074/jbc.M301981200
53. Zhang, H., Wang, Z., Wang, S., and Li, H. (2012). Progress of genome wide association study in domestic animals. J. Anim. Sci. Biotechnol. 3:26. doi: 10.1186/2049-1891-3-26