Genome-wide analytical approaches for reverse metabolic engineering of industrially relevant phenotypes in yeast

FEMS Yeast Research

Volumn 12, Issue 2, 2012, Pages 183-196

  Oud, Bart ^a   Van Maris, Antonius J A ^a   Daran, Jean Marc ^a   Pronk, Jack T ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

Evolutionary engineering; Inverse metabolic engineering; Systems biology; Transcriptomics; Whole genome sequencing; Yeast

Indexed keywords

PROTEOME; TRANSCRIPTOME;

COMPARATIVE GENOMIC HYBRIDIZATION; DNA MICROARRAY; DOWN REGULATION; GENE EXPRESSION; GENE SEQUENCE; GENETIC ASSOCIATION; GENOME ANALYSIS; METABOLIC ENGINEERING; METABOLOME; NONHUMAN; PHENOTYPE; PREDICTIVE VALUE; REVIEW; RNA SEQUENCE; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS; UPREGULATION; YEAST;

BIOLOGICAL EVOLUTION; BIOTECHNOLOGY; GENOME, FUNGAL; GENOME-WIDE ASSOCIATION STUDY; GENOMICS; METABOLIC ENGINEERING; MUTAGENESIS; PHENOTYPE; SACCHAROMYCES CEREVISIAE; TRANSCRIPTOME;

SACCHAROMYCES CEREVISIAE;

EID: 84857061668     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2011.00776.x     Document Type: Review

References (113)

1. Abbott DA, Knijnenburg TA, de Poorter LMI, Reinders MJT, Pronk JT & van Maris AJA (2007) Generic and specific transcriptional responses to different weak organic acids in anaerobic chemostat cultures of Saccharomyces cerevisiae. FEMS Yeast Res 7: 819-833.
2. Abbott DA, Zelle RM, Pronk JT & van Maris AJA (2009) Metabolic engineering of Saccharomyces cerevisiae for production of carboxylic acids: current status and challenges. FEMS Yeast Res 9: 1123-1136.
3. Alkan C, Coe BP & Eichler EE (2011) Genome structural variation discovery and genotyping. Nat Rev Genet 12: 363-376.
4. Alper H, Moxley J, Nevoigt E, Fink GR & Stephanopoulos G (2006) Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 314: 1565-1568.
5. Anderson JC, Dueber JE, Leguia M, Wu GC, Goler JA, Arkin AP & Keasling JD (2010) BglBricks: a flexible standard for biological part assembly. J Biol Eng 4: 1. DOI: 10.1186/1754-1611-4-1.
6. Araya CL, Payen C, Dunham MJ & Fields S (2010) Whole-genome sequencing of a laboratory-evolved yeast strain. BMC Genomics 11: 88. DOI: 10.1186/1471-2164-11-88.
7. Argueso JL, Carazzolle MF, Mieczkowski PA et al. (2009) Genome structure of a Saccharomyces cerevisiae strain widely used in bioethanol production. Genome Res 19: 2258-2270.
8. Bailey JE, Birnbaum S, Galazzo JL, Khosla C & Shanks JV (1990) Strategies and challenges in metabolic engineering. Ann N Y Acad Sci 589: 1-15.
9. Bailey JE, Sburlati A, Hatzimanikatis V, Lee K, Renner WA & Tsai PS (1996) Inverse metabolic engineering: a strategy for directed genetic engineering of useful phenotypes. Biotechnol Bioeng 52: 109-121.
10. Basso TO, de Kok S, Dario M et al. (2011) Engineering topology and kinetics of sucrose metabolism in Saccharomyces cerevisiae for improved ethanol yield. Metab Eng 13: 694-703.
11. Beck M, Claassen M & Aebersold R (2011) Comprehensive proteomics. Curr Opin Biotechnol 22: 3-8.
12. Becker J & Boles E (2003) A modified Saccharomyces cerevisiae strain that consumes l-arabinose and produces ethanol. Appl Environ Microbiol 69: 4144-4150.
13. Birrell GW, Brown JA, Wu HI, Giaever G, Chu AM, Davis RW & Brown JM (2002) Transcriptional response of Saccharomyces cerevisiae to DNA-damaging agents does not identify the genes that protect against these agents. P Natl Acad Sci USA 99: 8778-8783.
14. 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. J Biol Chem 278: 3265-3274.
15. Bro C & Nielsen J (2004) Impact of "ome" analyses on inverse metabolic engineering. Metab Eng 6: 204-211.
16. Bro C, Knudsen S, Regenberg B, Olsson L & Nielsen J (2005) Improvement of galactose uptake in Saccharomyces cerevisiae through overexpression of phosphoglucomutase: example of transcript analysis as a tool in inverse metabolic engineering. Appl Environ Microbiol 71: 6465-6472.
17. Brown CJ, Todd KM & Rosenzweig RF (1998) Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Mol Biol Evol 15: 931-942.
18. Casal M, Paiva S, Andrade RP, Gancedo C & Leão C (1999) The lactate-proton symport of Saccharomyces cerevisiae is encoded by JEN1. J Bacteriol 181: 2620-2623.
19. Castrillo JI, Zeef LA, Hoyle DC et al. (2007) Growth control of the eukaryote cell: a systems biology study in yeast. J Biol 6: 4. DOI: 10.1186/jbiol54.
20. Christen S & Sauer U (2011) Intracellular characterization of aerobic glucose metabolism in seven yeast species by 13C flux analysis and metabolomics. FEMS Yeast Res 11: 263-272.
21. Conrad TM, Lewis NE & Palsson BØ (2011) Microbial laboratory evolution in the era of genome-scale science. Mol Syst Biol 7: 509. DOI: 10.1038/msb.2011.42.
22. Cubillos FA, Billi E, Zörgö E, Parts L, Fargier P, Omholt S, Blomberg A, Warringer J, Louis EJ & Liti G (2011) Assessing the complex architecture of polygenic traits in diverged yeast populations. Mol Ecol 20: 1401-1413.
23. Daran-Lapujade P, Daran J, Kotter P, Petit T, Piper M & Pronk JT (2003) Comparative genotyping of the laboratory strains S288C and CEN.PK113-7D using oligonucleotide microarrays. FEMS Yeast Res 4: 259-269.
24. Daran-Lapujade P, Daran JM, van Maris AJA, de Winde JH & Pronk JT (2009) Chemostat-based micro-array analysis in baker's yeast. Adv Microb Physiol 54: 257-311.
25. de Groot MJL, Daran-Lapujade P, van Breukelen B, Knijnenburg TA, de Hulster EAF, Reinders MJT, Pronk JT, Heck AJR & Slijper M (2007) Quantitative proteomics and transcriptomics of anaerobic and aerobic yeast cultures reveals post-transcriptional regulation of key cellular processes. Microbiology 153: 3864-3878.
26. de Jesus Ferreira M, Bao X, Laizé V & Hohmann S (2001) Transposon mutagenesis reveals novel loci affecting tolerance to salt stress and growth at low temperature. Curr Genet 40: 27-39.
27. de Kok S, Nijkamp JF, Oud B, Roque FC, De Ridder D, Daran J.-M., Pronk JT & van Maris AJA (in press) Laboratory evolution of new lactate transporter genes in a jen1 mutant of Saccharomyces cerevisiae and their identification as ADY2 alleles by whole-genome resequencing and transcriptome analysis. FEMS Yeast Res, in press.
28. De Nicola R, Hazelwood LA, De Hulster EAF, Walsh MC, Knijnenburg TA, Reinders MJT, Walker GM, Pronk JT, Daran JM & Daran-Lapujade P (2007) Physiological and transcriptional responses of Saccharomyces cerevisiae to zinc limitation in chemostat cultures. Appl Environ Microbiol 73: 7680-7692.
29. DeRisi JL (1997) Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278: 680-686.
30. Dhar R, Sägesser R, Weikert C, Yuan J & Wagner A (2011) Adaptation of Saccharomyces cerevisiae to saline stress through laboratory evolution. J Evol Biol 24: 1135-1153.
31. Dunham MJ, Badrane H, Ferea T, Adams J, Brown PO, Rosenzweig F & Botstein D (2002) Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. P Natl Acad Sci USA 99: 16144-16149.
32. Duong CT, Strack L, Futschik M, Katou Y, Nakao Y, Fujimura T, Shirahige K, Kodama Y & Nevoigt E (2011) Identification of Sc-type ILV6 as a target to reduce diacetyl formation in lager brewers' yeast. Metab Eng 13: 638-647.
33. Ehrenreich IM, Torabi N, Jia Y, Kent J, Martis S, Shapiro JA, Gresham D, Caudy AA & Kruglyak L (2010) Dissection of genetically complex traits with extremely large pools of yeast segregants. Nature 464: 1039-1042.
34. Fazio A, Jewett MC, Daran-Lapujade P, Mustacchi R, Usaite R, Pronk JT, Workman CT & Nielsen J (2008) Transcription factor control of growth rate dependent genes in Saccharomyces cerevisiae: a three factor design. BMC Genomics 9: 341. DOI: 10.1186/1471-2164-9-341.
35. Ferea TL, Botstein D, Brown PO & Rosenzweig RF (1999) Systematic changes in gene expression patterns following adaptive evolution in yeast. P Natl Acad Sci USA 96: 9721-9726.
36. Giaever G, Flaherty P, Kumm J, Proctor M, Nislow C, Jaramillo DF, Chu AM, Jordan MI, Arkin AP & Davis RW (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
37. Giaever G, Flaherty P, Kumm J, Proctor M, Nislow C, Jaramillo DF, Chu AM, Jordan MI, Arkin AP & Davis RW (2004) Chemogenomic profiling: identifying the functional interactions of small molecules in yeast. P Natl Acad Sci USA 101: 793-798.
38. Gibson DG (2011) Gene and genome construction in yeast. Curr Protoc Mol Biol Chapter 3: Unit 3.22.
39. Goffeau A, Barrell BG, Bussey H et al. (1996) Life with 6000 genes. Science 274: 546, 563-567.
40. Gresham D, Ruderfer DM, Pratt SC, Schacherer J, Dunham MJ, Botstein D & Kruglyak L (2006) Genome-wide detection of polymorphisms at nucleotide resolution with a single DNA microarray. Science 311: 1932-1936.
41. Gresham D, Dunham M & Botstein D (2008a) Comparing whole genomes using DNA microarrays. Nat Rev Genet 9: 291-302.
42. Gresham D, Desai MM, Tucker CM, Jenq HT, Pai DA, Ward A, DeSevo CG, Botstein D & Dunham MJ (2008b) The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet 4: e1000303. DOI: 10.1371/journal.pgen.1000303.
43. Gresham D, Usaite R, Germann SM, Lisby M, Botstein D & Regenberg B (2010) Adaptation to diverse nitrogen-limited environments by deletion or extrachromosomal element formation of the GAP1 locus. P Natl Acad Sci USA 107: 18551-18556.
44. Hahn-Hägerdal B, Karhumaa K, Fonseca C, Spencer-Martins I & Gorwa-Grauslund MF (2007) Towards industrial pentose-fermenting yeast strains. Appl Environ Microbiol 74: 937-953.
45. Harbison CT, Gordon DB, Lee TI et al. (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431: 99-104.
46. Hong M-E, Lee K-S, Yu BJ, Sung Y-J, Park SM, Koo HM, Kweon D-H, Park JC & Jin Y-S (2010) Identification of gene targets eliciting improved alcohol tolerance in Saccharomyces cerevisiae through inverse metabolic engineering. J Biotechnol 149: 52-59.
47. Hong K-K, Vongsangnak W, Vemuri GN & Nielsen J (2011) Unravelling evolutionary strategies of yeast for improving galactose utilization through integrated systems level analysis. P Natl Acad Sci USA. DOI: 10.1073/pnas.1103219108.
48. Huang DW, Sherman BT & Lempicki RA (2009a) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13.
49. Huang DW, Sherman BT & Lempicki RA (2009b) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
50. Hughes SR, Gibbons WR, Bang SS et al. (2011) Random UV-C mutagenesis of Scheffersomyces (formerly Pichia) stipitis NRRL Y-7124 to improve anaerobic growth on lignocellulosic sugars. J Ind Microbiol Biotechnol. DOI: 10.1007/s10295-011-1012-x.
51. Jansen MLA, Diderich JA, Mashego M, Hassane A, de Winde JH, Daran-Lapujade P & Pronk JT (2005) Prolonged selection in aerobic, glucose-limited chemostat cultures of Saccharomyces cerevisiae causes a partial loss of glycolytic capacity. Microbiology 151: 1657-1669.
52. Jin Y-S, Alper H, Yang YT & Stephanopoulos G (2005) Improvement of xylose uptake and ethanol production in recombinant Saccharomyces cerevisiae through an inverse metabolic engineering approach. Society 71: 8249-8256.
53. Kao KC & Sherlock G (2008) Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat Genet 40: 1499-1504.
54. Karhumaa K, Påhlman AK, Hahn-Hägerdal B, Levander F & Gorwa-Grauslund MF (2009) Proteome analysis of the xylose-fermenting mutant yeast strain TMB 3400. Yeast 26: 371-382.
55. Kearsey M (1998) The principles of QTL analysis (a minimal mathematics approach). J Exp Bot 49: 1619-1623.
56. Kern A, Tilley E, Hunter IS, Legisa M & Glieder A (2007) Engineering primary metabolic pathways of industrial micro-organisms. J Biotechnol 129: 6-29.
57. Knijnenburg TA, Wessels LFA & Reinders MJT (2008) Combinatorial influence of environmental parameters on transcription factor activity. Bioinformatics 24: i172-i181.
58. Kolkman A, Slijper M & Heck AJR (2005) Development and application of proteomics technologies in Saccharomyces cerevisiae. Trends Biotechnol 23: 598-604.
59. Kresnowati MTAP, van Winden WA, Almering MJH, ten Pierick A, Ras C, Knijnenburg TA, Daran-Lapujade P, Pronk JT, Heijnen JJ & Daran JM (2006) When transcriptome meets metabolome: fast cellular responses of yeast to sudden relief of glucose limitation. Mol Syst Biol 2: 49. DOI: 10.1038/msb4100083.
60. Kvitek DJ & Sherlock G (2011) Reciprocal sign epistasis between frequently experimentally evolved adaptive mutations causes a rugged fitness landscape. Zhang J, ed. PLoS Genet 7: e1002056. DOI: 10.1371/journal.pgen.1002056
61. Lee JW, Kim TY, Jang Y-S, Choi S & Lee SY (2011) Systems metabolic engineering for chemicals and materials. Trends Biotechnol 29: 370-378.
62. Liti G, Haricharan S, Cubillos FA, Tierney AL, Sharp S, Bertuch AA, Parts L, Bailes E & Louis EJ (2009b) Segregating YKU80 and TLC1 alleles underlying natural variation in telomere properties in wild yeast. PLoS Genet 5: e1000659. DOI: 10.1371/journal.pgen.1000659.
63. MacIsaac KD, Wang T, Gordon DB, Gifford DK, Stormo GD & Fraenkel E (2006) An improved map of conserved regulatory sites for Saccharomyces cerevisiae. BMC Bioinformatics 7: 113. DOI: 10.1186/1471-2105-7-113.
64. Mardis ER (2006) Anticipating the 1, 000 dollar genome. Genome Biol 7: 112. DOI: 10.1186/gb-2006-7-7-112.
65. Mira NP, Palma M, Guerreiro JF & Sá-Correia I (2010) Genome-wide identification of Saccharomyces cerevisiae genes required for tolerance to acetic acid. Microb Cell Fact 9: 79. DOI: 10.1186/1475-2859-9-79.
66. Nevoigt E (2008) Progress in metabolic engineering of Saccharomyces cerevisiae. Microbiol Mol Biol Rev 72: 379-412.
67. Ni H, Laplaza JM & Jeffries TW (2007) Transposon mutagenesis to improve the growth of recombinant Saccharomyces cerevisiae on d-xylose. Appl Environ Microbiol 73: 2061-2066.
68. Nielsen J (1997) Physiological engineering aspects of Penicillium chrysogenum. World Scientific Publishing Co., Singapore.
69. Nielsen J (2001) Metabolic engineering. Appl Environ Microbiol 55: 263-283.
70. Nijkamp J, Winterbach W, van den Broek M, Daran JM, Reinders M & de Ridder D (2010) Integrating genome assemblies with MAIA. Bioinformatics 26: i433-i439.
71. Novo M, Bigey F, Beyne E et al. (2009) Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. P Natl Acad Sci USA 106: 16333-16338.
72. Olivares-Hernández R, Usaite R & Nielsen J (2010) Integrative analysis using proteome and transcriptome data from yeast to unravel regulatory patterns at post-transcriptional level. Biotechnol Bioeng 107: 865-875.
73. Ozsolak F & Milos PM (2011) RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 12: 87-98.
74. Parts L, Cubillos FA, Warringer J et al. (2011) Revealing the genetic structure of a trait by sequencing a population under selection. Genome Res 21: 1131-1138.
75. Petersson A, Almeida JRM, Modig T, Karhumaa K, Hahn-Hägerdal B, Gorwa-Grauslund MF & Lidén G (2006) A 5-hydroxymethyl furfural reducing enzyme encoded by the Saccharomyces cerevisiae ADH6 gene conveys HMF tolerance. Yeast 23: 455-464.
76. Pitkänen JP, Rintala E, Aristidou A, Ruohonen L & Penttilä M (2005) Xylose chemostat isolates of Saccharomyces cerevisiae show altered metabolite and enzyme levels compared with xylose, glucose, and ethanol metabolism of the original strain. Appl Environ Microbiol 67: 827-837.
77. Raynes Y, Gazzara MR & Sniegowski PD (2011) Mutator dynamics in sexual and asexual experimental populations of yeast. BMC Evol Biol 11: 158. DOI: 10.1186/1471-2148-11-158.
78. Regenberg B, Grotkjaer T, Winther O, Fausbøll A, Akesson M, Bro C, Hansen LK, Brunak S & Nielsen J (2006) Growth-rate regulated genes have profound impact on interpretation of transcriptome profiling in Saccharomyces cerevisiae. Genome Biol 7: R107. DOI: 10.1186/gb-2006-7-11-r107.
79. Rekoff M (1985) On reverse engineering. IEEE T Syst Man Cyb 15: 244-252.
80. Roessner U & Bowne J (2009) What is metabolomics all about? BioTechniques 46: 363-365.
81. Rossignol T, Kobi D, Jacquet-Gutfreund L & Blondin B (2009) The proteome of a wine yeast strain during fermentation, correlation with the transcriptome. J Appl Microbiol 107: 47-55.
82. Ross-Macdonald P, Coelho PS, Roemer T et al. (1999) Large-scale analysis of the yeast genome by transposon tagging and gene disruption. Nature 402: 413-418.
83. Rossouw D, van den Dool AH, Jacobson D & Bauer FF (2010) Comparative transcriptomic and proteomic profiling of industrial wine yeast strains. Appl Environ Microbiol 76: 3911-3923.
84. Sauer M, Porro D, Mattanovich D & Branduardi P (2010) 16 years research on lactic acid production with yeast - ready for the market? Biotechnol Genet Eng Rev 27: 229-256.
85. Schacherer J, Ruderfer DM, Gresham D, Dolinski K, Botstein D & Kruglyak L (2007) Genome-wide analysis of nucleotide-level variation in commonly used Saccharomyces cerevisiae strains. PLoS ONE 2: e322. DOI: 10.1371/journal.pone.0000322.
86. Schacherer J, Shapiro JA, Ruderfer DM & Kruglyak L (2009) Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458: 342-345.
87. Snoep JL, Yomano LP, Westerhoff HV & Ingram LO (1995) Protein burden in Zymomonas mobilis: negative flux and growth control due to overproduction of glycolytic enzymes. Microbiology 141: 2329-2337.
88. Sonderegger M & Sauer U (2003) Evolutionary engineering of Saccharomyces cerevisiae for anaerobic growth on xylose. Appl Environ Microbiol 69: 1990-1998.
89. Stanley D, Chambers PJ, Stanley GA, Borneman A & Fraser S (2010a) Transcriptional changes associated with ethanol tolerance in Saccharomyces cerevisiae. Appl Environ Microbiol 88: 231-239.
90. Stanley D, Fraser S, Chambers PJ, Rogers P & Stanley GA (2010b) Generation and characterisation of stable ethanol-tolerant mutants of Saccharomyces cerevisiae. J Ind Microbiol Biotechnol 37: 139-149.
91. Sutton J (1984) Reverse engineering the 80C86. Electron Eng 56: 51-54, 58.
92. Tai SL, Boer VM, Daran-Lapujade P, Walsh MC, de Winde JH, Daran JM & Pronk JT (2005) Two-dimensional transcriptome analysis in chemostat cultures. Combinatorial effects of oxygen availability and macronutrient limitation in Saccharomyces cerevisiae. J Biol Chem 280: 437-447.
93. Tai SL, Snoek I, Luttik MAH, Almering MJH, Walsh MC, Pronk JT & Daran JM (2007) Correlation between transcript profiles and fitness of deletion mutants in anaerobic chemostat cultures of Saccharomyces cerevisiae. Microbiology 153: 877-886.
94. Tanghe A, Van Dijck P, Dumortier F, Teunissen A, Hohmann S & Thevelein JM (2002) Aquaporin expression correlates with freeze tolerance in baker's yeast, and overexpression improves freeze tolerance in industrial strains. Appl Environ Microbiol 68: 5981-5989.
95. Thompson DA, Desai MM & Murray AW (2006) Ploidy controls the success of mutators and nature of mutations during budding yeast evolution. Curr Biol 16: 1581-1590.
96. Timmermann B, Jarolim S, Russmayer H, Kerick M, Michel S, Krüger A, Bluemlein K, Laun P, Grillari J, Lehrach H, Breitenbach M & Ralser M (2010) A new dominant peroxiredoxin allele identified by whole-genome re-sequencing of random mutagenized yeast causes oxidant-resistance and premature aging. Aging 2: 475-486.
97. Tsuruta H, Paddon CJ, Eng D, Lenihan JR, Horning T, Anthony LC, Regentin R, Keasling JD, Renninger NS & Newman JD (2009) High-level production of amorpha-4, 11-diene, a precursor of the antimalarial agent artemisinin, in Escherichia coli. PLoS ONE 4: e4489. DOI: 10.1371/journal.pone.0004489.
98. van den Berg MA, Albang R, Albermann K et al. (2008) Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat Biotechnol 26: 1161-1168.
99. van Maris AJA, Winkler AA, Kuyper M, de Laat WTAM, van Dijken JP & Pronk JT (2007) Development of efficient xylose fermentation in Saccharomyces cerevisiae: xylose isomerase as a key component. Adv Biochem Eng Biotechnol 108: 179-204.
100. 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. Appl Environ Microbiol 69: 740-746.
101. Wang HH, Isaacs FJ, Carr PA, Sun ZZ, Xu G, Forest CR & Church GM (2009a) Programming cells by multiplex genome engineering and accelerated evolution. Nature 460: 894-898.
102. Wang Z, Gerstein M & Snyder M (2009b) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10: 57-63.
103. Winzeler EA, Lee B, McCusker JH & Davis RW (1999a) Whole genome genetic-typing in yeast using high-density oligonucleotide arrays. Parasitology 118: S73-S80.
104. Winzeler EA, Shoemaker DD, Astromoff A et al. (1999b) Functional characterization of the Saccharomyces cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
105. Wisselink HW, Toirkens MJ, del Rosario Franco Berriel M, Winkler AA, van Dijken JP, Pronk JT & van Maris AJA (2007) Engineering of Saccharomyces cerevisiae for efficient anaerobic alcoholic fermentation of l-arabinose. Appl Environ Microbiol 73: 4881-4891.
106. Wisselink HW, Toirkens MJ, Wu Q, Pronk JT & van Maris AJA (2009) Novel evolutionary engineering approach for accelerated utilization of glucose, xylose, and arabinose mixtures by engineered Saccharomyces cerevisiae strains. Appl Environ Microbiol 75: 907-914.
107. Wisselink HW, Cipollina C, Oud B, Crimi B, Heijnen JJ, Pronk JT & van Maris AJA (2010) Metabolome, transcriptome and metabolic flux analysis of arabinose fermentation by engineered Saccharomyces cerevisiae. Metab Eng 12: 537-551.
108. Wright J, Bellissimi E, de Hulster E, Wagner A, Pronk JT & van Maris AJA (2011) Batch and continuous culture-based selection strategies for acetic acid tolerance in xylose-fermenting Saccharomyces cerevisiae. FEMS Yeast Res 11: 299-306.
109. Wu G, Nie L & Zhang W (2008) Integrative analyses of posttranscriptional regulation in the yeast Saccharomyces cerevisiae using transcriptomic and proteomic data. Curr Microbiol 57: 18-22.
110. Zaldivar J, Borges A, Johansson B, Smits HP, Villas-Bôas SG, Nielsen J & Olsson L (2002) Fermentation performance and intracellular metabolite patterns in laboratory and industrial xylose-fermenting Saccharomyces cerevisiae. Appl Environ Microbiol 59: 436-442.
111. Zelle RM, Trueheart J, Harrison JC, Pronk JT & van Maris AJA (2010) Phosphoenolpyruvate carboxykinase as the sole anaplerotic enzyme in Saccharomyces cerevisiae. Appl Environ Microbiol 76: 5383-5389.
112. Zelle RM, Harrison JC, Pronk JT & van Maris AJA (2011) Anaplerotic role for cytosolic malic enzyme in engineered Saccharomyces cerevisiae strains. Appl Environ Microbiol 77: 732-738.
113. Zhang F, Rodriguez S & Keasling JD (2011) Metabolic engineering of microbial pathways for advanced biofuels production. Curr Opin Biotechnol 22: 1-9.