Natural variation in non-coding regions underlying phenotypic diversity in budding yeast

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Salinas, Francisco ^a   De Boer, Carl G ^b   Abarca, Valentina ^c   García, Verónica ^c   Cuevas, Mara ^c   Araos, Sebastian ^c   Larrondo, Luis F ^a   Martínez, Claudio ^c   Cubillos, Francisco A ^a,c  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c UNIVERSIDAD DE SANTIAGO DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

ASN1 PROTEIN, S CEREVISIAE; ASPARTATE AMMONIA LIGASE; DNA BINDING PROTEIN; NITROGEN; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTION FACTOR; UGA3 PROTEIN, S CEREVISIAE;

ALLELE; CHIMERA; CROSS BREEDING; FUNGAL GENOME; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION STUDY; GENETIC VARIATION; GENETICS; INHERITANCE; METABOLISM; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PROMOTER REGION; QUANTITATIVE TRAIT LOCUS; SACCHAROMYCES CEREVISIAE;

ALLELES; ASPARTATE-AMMONIA LIGASE; BASE SEQUENCE; CHIMERA; CROSSES, GENETIC; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENETIC ASSOCIATION STUDIES; GENETIC VARIATION; GENOME, FUNGAL; INHERITANCE PATTERNS; NITROGEN; OPEN READING FRAMES; PROMOTER REGIONS, GENETIC; QUANTITATIVE TRAIT LOCI; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

EID: 84959017201     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep21849     Document Type: Article

References (64)

1. Mackay, T. F., Stone, E. A. & Ayroles, J. F. The genetics of quantitative traits: challenges and prospects. Nat Rev Genet 10, 565-577, doi: 10.1038/nrg2612 (2009).
2. Trontin, C., Tisne, S., Bach, L. & Loudet, O. What does Arabidopsis natural variation teach us (and does not teach us) about adaptation in plants? Curr Opin Plant Biol 14, 225-231, doi: 10.1016/j.pbi.2011.03.024 (2011).
3. Cubillos, F. A. et al. High-resolution mapping of complex traits with a four-parent advanced intercross yeast population. Genetics 195, 1141-1155, doi: 10.1534/genetics.113.155515 (2013).
4. Wei, P., Liu, X. & Fu, Y. X. Incorporating predicted functions of nonsynonymous variants into gene-based analysis of exome sequencing data: A comparative study. BMC Proc 5 Suppl 9, S20, doi: 10.1186/1753-6561-5-S9-S20 (2011).
5. Kumar, P., Henikoff, S. & Ng, P. C. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nature protocols 4, 1073-1081, doi: 10.1038/nprot.2009.86 (2009).
6. Parts, L. Genome-wide mapping of cellular traits using yeast. Yeast 31, 197-205, doi: 10.1002/yea.3010 (2014).
7. Fraser, H. B. et al. Polygenic cis-regulatory adaptation in the evolution of yeast pathogenicity. Genome Res 22, 1930-1939, doi: 10.1101/gr.134080.111 (2012).
8. Wray, G. A. The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 8, 206-216, doi: 10.1038/nrg2063 (2007).
9. Gerke, J., Lorenz, K. & Cohen, B. Genetic interactions between transcription factors cause natural variation in yeast. Science 323, 498-501, doi: 10.1126/science.1166426 (2009).
10. Majewski, J. & Pastinen, T. The study of eQTL variations by RNA-seq: from SNPs to phenotypes. Trends Genet 27, 72-79, doi: 10.1016/j.tig.2010.10.006 (2011).
11. Claussnitzer, M. et al. FTO Obesity Variant Circuitry and Adipocyte Browning in Humans. N Engl J Med, doi: 10.1056/NEJMoa1502214 (2015).
12. Smith, E. N. & Kruglyak, L. Gene-environment interaction in yeast gene expression. PLoS Biol 6, e83, doi: 10.1371/journal. pbio.0060083 (2008).
13. Kliebenstein, D. Quantitative genomics: Analyzing intraspecific variation using global gene expression polymorphisms or eQTLs. Annu Rev Plant Biol 60, 93-114, doi: 10.1146/annurev.arplant.043008.092114 (2009).
14. Cubillos, F. A. et al. Extensive cis-regulatory variation robust to environmental perturbation in Arabidopsis. Plant Cell 26, 4298-4310, doi: 10.1105/tpc.114.130310 (2014).
15. Goncalves, A. et al. Extensive compensatory cis-Trans regulation in the evolution of mouse gene expression. Genome research 22, 2376-2384, doi: 10.1101/gr.142281.112 (2012).
16. McManus, C. J. et al. Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Res 20, 816-825, doi: 10.1101/gr.102491.109 (2010).
17. Skelly, D. A., Johansson, M., Madeoy, J., Wakefield, J. & Akey, J. M. A powerful and flexible statistical framework for testing hypotheses of allele-specific gene expression from RNA-seq data. Genome research 21, 1728-1737, doi: 10.1101/gr.119784.110 (2011).
18. Lappalainen, T. et al. Transcriptome and genome sequencing uncovers functional variation in humans. Nature 501, 506-511, doi: 10.1038/nature12531 (2013).
19. Wittkopp, P. J. & Kalay, G. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet 13, 59-69, doi: 10.1038/nrg3095 (2012).
20. Chang, J. et al. The molecular mechanism of a cis-regulatory adaptation in yeast. PLoS Genet 9, e1003813, doi: 10.1371/journal. pgen.1003813 (2013).
21. Weirauch, M. T. et al. Determination and inference of eukaryotic transcription factor sequence specificity. Cell 158, 1431-1443, doi: 10.1016/j.cell.2014.08.009 (2014).
22. Baxter, I. et al. A coastal cline in sodium accumulation in Arabidopsis thaliana is driven by natural variation of the sodium transporter AtHKT1;1. PLoS genetics 6, e1001193, doi: 10.1371/journal.pgen.1001193 (2010).
23. Westra, H. J. et al. Systematic identification of trans eQTLs as putative drivers of known disease associations. Nat Genet 45, 1238-1243, doi: 10.1038/ng.2756 (2013).
24. Fay, J. C., McCullough, H. L., Sniegowski, P. D. & Eisen, M. B. Population genetic variation in gene expression is associated with phenotypic variation in Saccharomyces cerevisiae. Genome Biol 5, R26, doi: 10.1186/gb-2004-5-4-r26 (2004).
25. Liti, G. et al. Population genomics of domestic and wild yeasts. Nature 458, 337-341, doi: 10.1038/nature07743 (2009).
26. Bergstrom, A. et al. A high-definition view of functional genetic variation from natural yeast genomes. Mol Biol Evol 31, 872-888, doi: 10.1093/molbev/msu037 (2014).
27. Warringer, J. et al. Trait variation in yeast is defined by population history. PLoS Genet 7, e1002111, doi: 10.1371/journal. pgen.1002111 (2011).
28. de Boer, C. G. & Hughes, T. R. YeTFaSCo: A database of evaluated yeast transcription factor sequence specificities. Nucleic Acids Res 40, D169-179, doi: 10.1093/nar/gkr993 (2012).
29. MacPherson, S., Larochelle, M. & Turcotte, B. A fungal family of transcriptional regulators: The zinc cluster proteins. Microbiol Mol Biol Rev 70, 583-604, doi: 10.1128/MMBR.00015-06 (2006).
30. Talibi, D., Grenson, M. & Andre, B. Cis-And trans-Acting elements determining induction of the genes of the gamma-Aminobutyrate (GABA) utilization pathway in Saccharomyces cerevisiae. Nucleic Acids Res 23, 550-557 (1995).
31. Xie, J. et al. Sum1 and Hst1 repress middle sporulation-specific gene expression during mitosis in Saccharomyces cerevisiae. EMBO J 18, 6448-6454, doi: 10.1093/emboj/18.22.6448 (1999).
32. Liu, H., Styles, C. A. & Fink, G. R. Elements of the yeast pheromone response pathway required for filamentous growth of diploids. Science 262, 1741-1744 (1993).
33. Errede, B. & Ammerer, G. STE12, a protein involved in cell-Type-specific transcription and signal transduction in yeast, is part of protein-DNA complexes. Genes Dev 3, 1349-1361 (1989).
34. Gimeno, C. J. & Fink, G. R. Induction of pseudohyphal growth by overexpression of PHD1, a Saccharomyces cerevisiae gene related to transcriptional regulators of fungal development. Mol Cell Biol 14, 2100-2112 (1994).
35. Ashburner, M. et al. Gene ontology: Tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25, 25-29, doi: 10.1038/75556 (2000).
36. Kanehisa, M. & Goto, S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28, 27-30 (2000).
37. Ambroset, C. et al. Deciphering the molecular basis of wine yeast fermentation traits using a combined genetic and genomic approach. G3 (Bethesda) 1, 263-281, doi: 10.1534/g3.111.000422 (2011).
38. Pigeau, G. M. & Inglis, D. L. Response of wine yeast (Saccharomyces cerevisiae) aldehyde dehydrogenases to acetaldehyde stress during Icewine fermentation. J Appl Microbiol 103, 1576-1586, doi: 10.1111/j.1365-2672.2007.03381.x (2007).
39. Nissen, T. L., Kielland-Brandt, M. C., Nielsen, J. & Villadsen, J. Optimization of ethanol production in Saccharomyces cerevisiae by metabolic engineering of the ammonium assimilation. Metab Eng 2, 69-77, doi: 10.1006/mben.1999.0140 (2000).
40. Piddocke, M. P. et al. Revealing the beneficial effect of protease supplementation to high gravity beer fermentations using "-omics" techniques. Microb Cell Fact 10, 27, doi: 10.1186/1475-2859-10-27 (2011).
41. Albert, F. W., Muzzey, D., Weissman, J. S. & Kruglyak, L. Genetic influences on translation in yeast. PLoS Genet 10, e1004692, doi: 10.1371/journal.pgen.1004692 (2014).
42. Brem, R. B., Yvert, G., Clinton, R. & Kruglyak, L. Genetic dissection of transcriptional regulation in budding yeast. Science 296, 752-755, doi: 10.1126/science.1069516 (2002).
43. Kemmeren, P. et al. Large-scale genetic perturbations reveal regulatory networks and an abundance of gene-specific repressors. Cell 157, 740-752, doi: 10.1016/j.cell.2014.02.054 (2014).
44. Foster, H. A. et al. The zinc cluster protein Sut1 contributes to filamentation in Saccharomyces cerevisiae. Eukaryot Cell 12, 244-253, doi: 10.1128/EC.00214-12 (2013).
45. Hope, E. A. & Dunham, M. J. Ploidy-regulated variation in biofilm-related phenotypes in natural isolates of Saccharomyces cerevisiae. G3 (Bethesda) 4, 1773-1786, doi: 10.1534/g3.114.013250 (2014).
46. Costanzo, M. et al. The genetic landscape of a cell. Science 327, 425-431, doi: 10.1126/science.1180823 (2010).
47. Bullard, J. H., Mostovoy, Y., Dudoit, S. & Brem, R. B. Polygenic and directional regulatory evolution across pathways in Saccharomyces. Proc Natl Acad Sci USA 107, 5058-5063, doi: 10.1073/pnas.0912959107 (2010).
48. Martin, H. C., Roop, J. I., Schraiber, J. G., Hsu, T. Y. & Brem, R. B. Evolution of a membrane protein regulon in Saccharomyces. Mol Biol Evol 29, 1747-1756, doi: 10.1093/molbev/mss017 (2012).
49. Cubillos, F. A. et al. Assessing the complex architecture of polygenic traits in diverged yeast populations. Mol Ecol, doi: 10.1111/j.1365-294X.2011.05005.x (2011).
50. Kent, W. J. BLAT-The BLAST-like alignment tool. Genome Res 12, 656-664, doi: 10.1101/gr.229202. Article published online before March 2002 (2002).
51. Li, B. & Dewey, C. N. RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323, doi: 10.1186/1471-2105-12-323 (2011).
52. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10, R25, doi: 10.1186/gb-2009-10-3-r25 (2009).
53. Storey, J. D. & Tibshirani, R. Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100, 9440-9445, doi: 10.1073/pnas.1530509100 (2003).
54. Granek, J. A. & Clarke, N. D. Explicit equilibrium modeling of transcription-factor binding and gene regulation. Genome Biol 6, R87, doi: 10.1186/gb-2005-6-10-r87 (2005).
55. Huang da, W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4, 44-57, doi: 10.1038/nprot.2008.211 (2009).
56. Jara, M. et al. Mapping genetic variants underlying differences in the central nitrogen metabolism in fermenter yeasts. PLoS One 9, e86533, doi: 10.1371/journal.pone.0086533 (2014).
57. Salinas, F. et al. The Genetic Basis of Natural Variation in Oenological Traits in Saccharomyces cerevisiae. PLoS One 7, e49640, doi: 10.1371/journal.pone.0049640 (2012).
58. Cubillos, F. A., Louis, E. J. & Liti, G. Generation of a large set of genetically tractable haploid and diploid Saccharomyces strains. FEMS Yeast Res 9, 1217-1225, doi: 10.1111/j.1567-1364.2009.00583.x (2009).
59. Huxley, C., Green, E. D. & Dunham, I. Rapid assessment of S. cerevisiae mating type by PCR. Trends in genetics : TIG 6, 236 (1990).
60. Oldenburg, K. R., Vo, K. T., Michaelis, S. & Paddon, C. Recombination-mediated PCR-directed plasmid construction in vivo in yeast. Nucleic Acids Res 25, 451-452 (1997).
61. Gibson, D. G. et al. One-step assembly in yeast of 25 overlapping DNA fragments to form a complete synthetic Mycoplasma genitalium genome. Proc Natl Acad Sci USA 105, 20404-20409, doi: 10.1073/pnas.0811011106 (2008).
62. Rossignol, T., Dulau, L., Julien, A. & Blondin, B. Genome-wide monitoring of wine yeast gene expression during alcoholic fermentation. Yeast 20, 1369-1385, doi: 10.1002/yea.1046 (2003).
63. Gomez-Alonso, S., Hermosin-Gutierrez, I. & Garcia-Romero, E. Simultaneous HPLC analysis of biogenic amines, amino acids, and ammonium ion as aminoenone derivatives in wine and beer samples. J Agric Food Chem 55, 608-613, doi: 10.1021/jf062820m (2007).
64. Rienzo, A., Pascual-Ahuir, A. & Proft, M. The use of a real-Time luciferase assay to quantify gene expression dynamics in the living yeast cell. Yeast 29, 219-231, doi: 10.1002/yea.2905 (2012).