Genetic Basis of Metabolome Variation in Yeast

PLoS Genetics

Volumn 10, Issue 3, 2014, Pages

  Breunig, Jeffrey S ^a   Hackett, Sean R ^a   Rabinowitz, Joshua D ^a   Kruglyak, Leonid ^b,c  

^a PRINCETON UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

S ADENOSYLHOMOCYSTEINE; S ADENOSYLMETHIONINE;

ARTICLE; CELL WALL; CONTROLLED STUDY; DNA POLYMORPHISM; ERC1 GENE; FUNGAL GENE; GENE DELETION; GENE FREQUENCY; GENE LOCUS; GENE SEGREGATION; GENETIC VARIABILITY; GLUCOSE TRANSPORT; HERITABILITY; LINKAGE ANALYSIS; LIQUID CHROMATOGRAPHY; METABOLOME; NONHUMAN; QUANTITATIVE TRAIT LOCUS; SACCHAROMYCES CEREVISIAE; SLT2 GENE; TANDEM MASS SPECTROMETRY; URA3 GENE; YEAST; CARBOHYDRATE METABOLISM; GENETIC LINKAGE; GENETICS; METABOLISM; METABOLOMICS;

CARBOHYDRATE METABOLISM; CHROMATOGRAPHY, LIQUID; GENETIC LINKAGE; METABOLOME; METABOLOMICS; QUANTITATIVE TRAIT LOCI; SACCHAROMYCES CEREVISIAE; TANDEM MASS SPECTROMETRY;

EID: 84897455911     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004142     Document Type: Article

References (73)

1. Bijlsma S, Bobeldijk I, Verheij ER, Ramaker R, (2006) Large-scale human metabolomics studies: a strategy for data (pre-) processing and validation. Analytical Chemistry 78: 567-574.
2. Sladek R, Rocheleau G, Rung J, Dina C, Shen L, et al. (2007) A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature 445: 881-885.
3. Marchesi JR, Holmes E, Khan F, Kochhar S, Scanlan P, et al. (2007) Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. Journal of proteome research 6: 546-551.
4. Swiegers JH, Pretorius IS (2005) Yeast Modulation of Wine Flavor. In: Advances in applied microbiology, Elsevier. pp. 131-175.
5. Keasling JD, Chou H, (2008) Metabolic engineering delivers next-generation biofuels. Nature Publishing Group 26: 298-299.
6. Wahlbom CF, Cordero Otero RR, van Zyl WH, Hahn-Hägerdal B, Jönsson LJ, (2003) Molecular analysis of a Saccharomyces cerevisiae mutant with improved ability to utilize xylose shows enhanced expression of proteins involved in transport, initial xylose metabolism, and the pentose phosphate pathway. Applied and environmental microbiology 69: 740-746.
7. Fiehn O, (2002) Metabolomics-the link between genotypes and phenotypes. Plant molecular biology 48: 155-171.
8. Goodacre R, Vaidyanathan S, Dunn WB, Harrigan GG, Kell DB, (2004) Metabolomics by numbers: acquiring and understanding global metabolite data. Trends in biotechnology 22: 245-252.
9. Hall RD, (2006) Plant metabolomics: from holistic hope, to hype, to hot topic. The New phytologist 169: 453-468.
10. Schauer N, Fernie AR, (2006) Plant metabolomics: towards biological function and mechanism. Trends in plant science 11: 508-516.
11. Allen J, Davey HM, Broadhurst D, Heald JK, Rowland JJ, et al. (2003) High-throughput classification of yeast mutants for functional genomics using metabolic footprinting. Nature Biotechnology 21: 692-696.
12. Benfey PN, Mitchell-Olds T, (2008) From genotype to phenotype: systems biology meets natural variation. Science 320: 495-497.
13. Villas-Bôas SG, Moxley JF, Akesson M, Stephanopoulos G, Nielsen J, (2005) Highthroughput metabolic state analysis: the missing link in integrated functional genomics of yeasts. The Biochemical journal 388: 669-677.
14. Smedsgaard J, Nielsen J, (2005) Metabolite profiling of fungi and yeast: from phenotype to metabolome by MS and informatics. Journal of experimental botany 56: 273-286.
15. Clasquin MF, Melamud E, Singer A, Gooding JR, Xu X, et al. (2011) Riboneogenesis in yeast. Cell 145: 969-980.
16. DellaPenna D, Last RL, (2008) Genome-enabled approaches shed new light on plant metabolism. Science 320: 479-481.
17. McMullen MD, Byrne PF, Snook ME, Wiseman BR, Lee EA, et al. (1998) Quantitative trait loci and metabolic pathways. Proceedings of the National Academy of Sciences of the United States of America 95: 1996-2000.
18. Bost B, Dillmann C, de Vienne D, (1999) Fluxes and metabolic pools as model traits for quantitative genetics. I. The L-shaped distribution of gene effects. Genetics 153: 2001-2012.
19. Mitchell-Olds T, Pedersen D, (1998) The molecular basis of quantitative genetic variation in central and secondary metabolism in Arabidopsis. Genetics 149: 739-747.
20. Keurentjes JJB, Fu J, de Vos CHR, Lommen A, Hall RD, et al. (2006) The genetics of plant metabolism. Nature Genetics 38: 842-849.
21. Lisec J, Meyer RC, Steinfath M, Redestig H, Becher M, et al. (2008) Identification of metabolic and biomass QTL in Arabidopsis thaliana in a parallel analysis of RIL and IL populations. The Plant journal: for cell and molecular biology 53: 960-972.
22. Bentsink L, Alonso-Blanco C, Vreugdenhil D, Tesnier K, Groot SP, et al. (2000) Genetic analysis of seed-soluble oligosaccharides in relation to seed storability of Arabidopsis. Plant physiology 124: 1595-1604.
23. Hobbs DH, Flintham JE, Hills MJ, (2004) Genetic control of storage oil synthesis in seeds of Arabidopsis. Plant physiology 136: 3341-3349.
24. Kliebenstein DJ, Gershenzon J, Mitchell-Olds T, (2001) Comparative quantitative trait loci mapping of aliphatic, indolic and benzylic glucosinolate production in Arabidopsis thaliana leaves and seeds. Genetics 159: 359-370.
25. Wentzell AM, Rowe HC, Hansen BG, Ticconi C, Halkier BA, et al. (2007) Linking metabolic QTLs with network and cis-eQTLs controlling biosynthetic pathways. PLoS Genetics 3: 1687-1701.
26. Dumas ME, Wilder SP, Bihoreau MT, Barton RH, Fearnside JF, et al. (2007) Direct quantitative trait locus mapping of mammalian metabolic phenotypes in diabetic and normoglycemic rat models. Nature Genetics 39: 666-672.
27. Rowe HC, Hansen BG, Halkier BA, (2008) Biochemical networks and epistasis shape the Arabidopsis thaliana metabolome. Plant Cell 20: 1199-1216.
28. Zhu J, Sova P, Xu Q, Dombek KM, Xu EY, et al. (2012) Stitching together Multiple Data Dimensions Reveals Interacting Metabolomic and Transcriptomic Networks That Modulate Cell Regulation. PLoS Biology 10: e1001301.
29. Smith EN, Kruglyak L, (2008) Gene-Environment Interaction in Yeast Gene Expression. PLoS Biology 6: 810-824.
30. Foss EJ, Radulovic D, Shaffer SA, Ruderfer DM, Bedalov A, et al. (2007) Genetic basis of proteome variation in yeast. Nature Genetics 39: 1369-1375.
31. Brem RB, Storey JD, Whittle J, Kruglyak L, (2005) Genetic interactions between polymorphisms that affect gene expression in yeast. Nature 436: 701-703.
32. Brem RB, Kruglyak L, (2005) The landscape of genetic complexity across 5,700 gene expression traits in yeast. Proceedings of the National Academy of Sciences of the United States of America 102: 1572-1577.
33. Perlstein EO, Ruderfer DM, Roberts DC, Schreiber SL, Kruglyak L, (2007) Genetic basis of individual differences in the response to small-molecule drugs in yeast. Nature Genetics 39: 496-502.
34. Perlstein EO, Ruderfer DM, Ramachandran G, Haggarty SJ, Kruglyak L, et al. (2006) Revealing complex traits with small molecules and naturally recombinant yeast strains. Chemistry & biology 13: 319-327.
35. Brauer MJ, Yuan J, Bennett BD, Lu W, Kimball E, et al. (2006) Conservation of the metabolomic response to starvation across two divergent microbes. Proceedings of the National Academy of Sciences of the United States of America 103: 19302-19307.
36. Lu W, Bennett BD, Rabinowitz JD, (2008) Analytical strategies for LC-MS-based targeted metabolomics. Journal of chromatography B, Analytical technologies in the biomedical and life sciences 871: 236-242.
37. Storey JD, Tibshirani R, (2003) Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences of the United States of America 100: 9440-9445.
38. Broman KW, Wu H, Sen Ś, Churchill GA, (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19: 889-890.
39. Kampfer AJ, Balog EM, (2010) S-adenosyl-L-methionine regulation of the cardiac ryanodine receptor involves multiple mechanisms. Biochemistry 49: 7600-7614.
40. Fetrow CW, Avila JR, (2001) Efficacy of the dietary supplement S-adenosyl-Lmethionine. The Annals of pharmacotherapy 35: 1414-1425.
41. Mo ML, Palsson BØ, Herrgard MJ, (2009) Connecting extracellular metabolomic measurements to intracellular flux states in yeast. BMC Systems Biology 3: 37.
42. de Llanos R, Herńandez-Haro C, Barrio E, Querol A, Ferńandez-Espinar MT, et al. (2010) Differences in activation of MAP kinases and variability in the polyglutamine tract of Slt2 in clinical and non-clinical isolates of Saccharomyces cerevisiae. Yeast (Chichester, England) 27: 549-561.
43. Choi ES, Park BS, Lee SW, Oh MK, (2009) Increased production of S-adenosyl-Lmethionine using recombinant Saccharomyces cerevisiae sake K6. Korean Journal of Chemical Engineering 26: 156-159.
44. Lee SW, Park BS, Choi ES, Oh MK, (2010) Overexpression of ethionine resistance gene for maximized production of S-adenosylmethionine in Saccharomyces cerevisiae sake kyokai No. 6. Korean Journal of Chemical Engineering 27: 587-589.
45. Shiomi N, Fukuda H, Fukuda Y, Murata K, (1991) Nucleotide sequence and characterization of a Gene conferring resistance to ethionine in yeast Saccharomyces cerevisiae. Journal of Fermentation and Bioengineering 71: 211-215.
46. Tanaka K, Lin BK, Wood DR, Tamanoi F, (1991) IRA2, an upstream negative regulator of RAS in yeast, is a RAS GTPase-activating protein. Proceedings of the National Academy of Sciences of the United States of America 88: 468-472.
47. Kim JW, Dang CV, (2006) Cancer's molecular sweet tooth and the Warburg effect. Cancer research 66: 8927-8930.
48. Storey JD, Akey JM, Kruglyak L, (2005) Multiple locus linkage analysis of genomewide expression in yeast. PLoS Biology 3: e267.
49. Parrini MC, Jacquet E, Bernardi A, Jacquet M, Parmeggiani A, (1995) Properties and regulation of the catalytic domain of Ira2p, a Saccharomyces cerevisiae GTPase-activating protein of Ras2p. Biochemistry 34: 13776-13783.
50. Broach JR, (1991) RAS genes in Saccharomyces cerevisiae: signal transduction in search of a pathway. Trends in genetics: TIG 7: 28-33.
51. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, 1 edition.
52. West MAL, Kim K, Kliebenstein DJ, van Leeuwen H, Michelmore RW, et al. (2006) Global eQTL Mapping Reveals the Complex Genetic Architecture of Transcript-Level Variation in Arabidopsis. Genetics 175: 1441-1450.
53. Bloom JS, Ehrenreich IM, Loo WT, Lite TLV, Kruglyak L, (2013) Finding the sources of missing heritability in a yeast cross. Nature 494: 234-237.
54. Mato JM, Corrales FJ, Lu SC, (2002) AvilaMA (2002) S-Adenosylmethionine: a control switch that regulates liver function. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 16: 15-26.
55. Mischoulon D, Fava M, (2002) Role of S-adenosyl-L-methionine in the treatment of depression: a review of the evidence. The American journal of clinical nutrition 76: 1158S-61S.
56. Rème CA, Dramard V, Kern L, Hofmans J, Halsberghe C, et al. (2008) Effect of Sadenosylmethionine tablets on the reduction of age-related mental decline in dogs: a double-blinded, placebo-controlled trial. Veterinary therapeutics: research in applied veterinary medicine 9: 69-82.
57. Fuso A, Seminara L, Cavallaro RA, D'Anselmi F, (2005) Sadenosylmethionine/homocysteine cycle alterations modify DNA methylation status with consequent deregulation of PS1 and BACE and beta-amyloid production. Molecular and Cellular Neuroscience 28: 154-204.
58. Martin-Yken H, Dagkessamanskaia A, Basmaji F, Lagorce A, Francois J, (2003) The interaction of Slt2 MAP kinase with Knr4 is necessary for signalling through the cell wall integrity pathway in Saccharomyces cerevisiae. Molecular microbiology 49: 23-35.
59. Chen Y, Feldman DE, Deng C, Brown JA, De Giacomo AF, et al. (2005) Identification of mitogen-activated protein kinase signaling pathways that confer resistance to endoplasmic reticulum stress in Saccharomyces cerevisiae. Molecular cancer research: MCR 3: 669-677.
60. Lesage G, Bussey H, (2006) Cell wall assembly in Saccharomyces cerevisiae. Microbiology and molecular biology reviews: MMBR 70: 317-343.
61. Boer VM, de Winde JH, Pronk JT, Piper MDW, (2003) The Genome-wide Transcriptional Responses of Saccharomyces cerevisiae Grown on Glucose in Aerobic Chemostat Cultures Limited for Carbon, Nitrogen, Phosphorus, or Sulfur. The Journal of biological chemistry 278: 3265-3274.
62. Cavalieri D, Townsend JP, Hartl DL, (2000) Manifold anomalies in gene expression in a vineyard isolate of Saccharomyces cerevisiae revealed by DNA microarray analysis. Proceedings of the National Academy of Sciences of the United States of America 97: 12369-12374.
63. Madden K, Sheu YJ, Baetz K, Andrews B, Snyder M, (1997) SBF Cell Cycle Regulator as a Target of the Yeast PKC-MAP Kinase Pathway. Science 275: 1781-1784.
64. Blank HM, Gajjar S, Belyanin A, Polymenis M, (2009) Sulfur metabolism actively promotes initiation of cell division in yeast. PloS one 4: e8018.
65. Tu BP, Kudlicki A, Rowicka M, McKnight SL, (2005) Logic of the Yeast Metabolic Cycle: Temporal Compartmentalization of Cellular Processes. Science 310: 1152-1158.
66. Tu BP, McKnight SL, (2006) Metabolic cycles as an underlying basis of biological oscillations. Nature reviews Molecular cell biology 7: 696-701.
67. Tu BP, Mohler RE, Liu JC, Dombek KM, Young ET, et al. (2007) Cyclic changes in metabolic state during the life of a yeast cell. Proceedings of the National Academy of Sciences of the United States of America 104: 16886-16891.
68. Kruglyak L, Lander ES, (1995) A nonparametric approach for mapping quantitative trait loci. Genetics 139: 1421-1428.
69. Bajad SU, Lu W, Kimball EH, Yuan J, Peterson C, et al. (2006) Separation and quantitation of water soluble cellular metabolites by hydrophilic interaction chromatographytandem mass spectrometry. Journal of chromatography A 1125: 76-88.
70. Luo B, Groenke K, Takors R, Wandrey C, Oldiges M, (2007) Simultaneous determination of multiple intracellular metabolites in glycolysis, pentose phosphate pathway and tricarboxylic acid cycle by liquid chromatography-mass spectrometry. Journal of chromatography A 1147: 153-164.
71. Melamud E, Vastag L, Rabinowitz JD, (2010) Metabolomic Analysis and Visualization Engine for LC-MS Data. Analytical Chemistry 82: 9818-9826.
72. Gray M, Piccirillo S, Honigberg SM, (2005) Two-step method for constructing unmarked insertions, deletions and allele substitutions in the yeast genome. FEMS microbiology letters 248: 31-36.
73. Davison AC, Hinkley DV (1997) Bootstrap Methods and their Application. Cambridge University Press.