Reverse Evolution of a Classic Gene Network in Yeast Offers a Competitive Advantage

Current Biology

Volumn 29, Issue 7, 2019, Pages 1126-1136.e5

  Duan, Shou Fu ^a,b   Shi, Jun Yan ^a,b   Yin, Qi ^a,b   Zhang, Ri Peng ^a,b   Han, Pei Jie ^a   Wang, Qi Ming ^a   Bai, Feng Yan ^a,b  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

ecological adaptation; GAL network; glucose repression; introgression; reverse evolution; Saccharomyces cerevisiae; yeast

Indexed keywords

GLUCOSE;

FUNGAL GENE; GENE REGULATORY NETWORK; GENETICS; METABOLISM; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

BASE SEQUENCE; EVOLUTION, MOLECULAR; GENE REGULATORY NETWORKS; GENES, FUNGAL; GLUCOSE; SACCHAROMYCES CEREVISIAE;

EID: 85063338699     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2019.02.038     Document Type: Article

References (67)

1. Gancedo, J.M., Yeast carbon catabolite repression. Microbiol. Mol. Biol. Rev. 62 (1998), 334–361.
2. Görke, B., Stülke, J., Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat. Rev. Microbiol. 6 (2008), 613–624.
3. Vinuselvi, P., Kim, M.K., Lee, S.K., Ghim, C.M., Rewiring carbon catabolite repression for microbial cell factory. BMB Rep. 45 (2012), 59–70.
4. Johnston, M., Feasting, fasting and fermenting. Glucose sensing in yeast and other cells. Trends Genet. 15 (1999), 29–33.
5. Ronne, H., Glucose repression in fungi. Trends Genet. 11 (1995), 12–17.
6. Carlson, M., Glucose repression in yeast. Curr. Opin. Microbiol. 2 (1999), 202–207.
7. Piškur, J., Rozpedowska, E., Polakova, S., Merico, A., Compagno, C., How did Saccharomyces evolve to become a good brewer?. Trends Genet. 22 (2006), 183–186.
8. Dashko, S., Zhou, N., Compagno, C., Piškur, J., Why, when, and how did yeast evolve alcoholic fermentation?. FEMS Yeast Res. 14 (2014), 826–832.
9. Diaz-Ruiz, R., Rigoulet, M., Devin, A., The Warburg and Crabtree effects: on the origin of cancer cell energy metabolism and of yeast glucose repression. Biochim. Biophys. Acta 1807 (2011), 568–576.
10. Hagman, A., Säll, T., Compagno, C., Piškur, J., Yeast “make-accumulate-consume” life strategy evolved as a multi-step process that predates the whole genome duplication. PLoS ONE, 8, 2013, e68734.
11. Sun, G., Dilcher, D.L., Wang, H., Chen, Z., A eudicot from the early cretaceous of China. Nature 471 (2011), 625–628.
12. Kayikci, Ö., Nielsen, J., Glucose repression in Saccharomyces cerevisiae. FEMS Yeast Res., 15, 2015, fov068.
13. Rolland, F., Winderickx, J., Thevelein, J.M., Glucose-sensing mechanisms in eukaryotic cells. Trends Biochem. Sci. 26 (2001), 310–317.
14. Rolland, F., Winderickx, J., Thevelein, J.M., Glucose-sensing and -signalling mechanisms in yeast. FEMS Yeast Res. 2 (2002), 183–201.
15. Santangelo, G.M., Glucose signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 70 (2006), 253–282.
16. Jarosz, D.F., Brown, J.C.S., Walker, G.A., Datta, M.S., Ung, W.L., Lancaster, A.K., Rotem, A., Chang, A., Newby, G.A., Weitz, D.A., et al. Cross-kingdom chemical communication drives a heritable, mutually beneficial prion-based transformation of metabolism. Cell 158 (2014), 1083–1093.
17. Jarosz, D.F., Lancaster, A.K., Brown, J.C.S., Lindquist, S., An evolutionarily conserved prion-like element converts wild fungi from metabolic specialists to generalists. Cell 158 (2014), 1072–1082.
18. Garcia, D.M., Dietrich, D., Clardy, J., Jarosz, D.F., A common bacterial metabolite elicits prion-based bypass of glucose repression. eLife, 5, 2016, e17978.
19. Johnston, M., A model fungal gene regulatory mechanism: the GAL genes of Saccharomyces cerevisiae. Microbiol. Rev. 51 (1987), 458–476.
20. Horák, J., Regulations of sugar transporters: insights from yeast. Curr. Genet. 59 (2013), 1–31.
21. Duan, S.F., Han, P.J., Wang, Q.M., Liu, W.Q., Shi, J.Y., Li, K., Zhang, X.L., Bai, F.Y., The origin and adaptive evolution of domesticated populations of yeast from Far East Asia. Nat. Commun. 9 (2018), 2690–2702.
22. Ball, A.J., Wong, D.K., Elliott, J.J., Glucosamine resistance in yeast. I. A preliminary genetic analysis. Genetics 84 (1976), 311–317.
23. Kunz, B.A., Ball, A.J., Glucosamine resistance in yeast. II. Cytoplasmic determinants conferring resistance. Mol. Gen. Genet. 153 (1977), 169–177.
24. Yano, K., Fukasawa, T., Galactose-dependent reversible interaction of Gal3p with Gal80p in the induction pathway of Gal4p-activated genes of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 94 (1997), 1721–1726.
25. Suzuki-Fujimoto, T., Fukuma, M., Yano, K.I., Sakurai, H., Vonika, A., Johnston, S.A., Fukasawa, T., Analysis of the galactose signal transduction pathway in Saccharomyces cerevisiae: interaction between Gal3p and Gal80p. Mol. Cell. Biol. 16 (1996), 2504–2508.
26. Ostergaard, S., Walløe, K.O., Gomes, S.G., Olsson, L., Nielsen, J., The impact of GAL6, GAL80, and MIG1 on glucose control of the GAL system in Saccharomyces cerevisiae. FEMS Yeast Res. 1 (2001), 47–55.
27. Stockwell, S.R., Landry, C.R., Rifkin, S.A., The yeast galactose network as a quantitative model for cellular memory. Mol. Biosyst. 11 (2015), 28–37.
28. Nehlin, J.O., Carlberg, M., Ronne, H., Control of yeast GAL genes by MIG1 repressor: a transcriptional cascade in the glucose response. EMBO J. 10 (1991), 3373–3377.
29. Griggs, D.W., Johnston, M., Regulated expression of the GAL4 activator gene in yeast provides a sensitive genetic switch for glucose repression. Proc. Natl. Acad. Sci. USA 88 (1991), 8597–8601.
30. Lundin, M., Nehlin, J.O., Ronne, H., Importance of a flanking AT-rich region in target site recognition by the GC box-binding zinc finger protein MIG1. Mol. Cell. Biol. 14 (1994), 1979–1985.
31. Platt, A., Reece, R.J., The yeast galactose genetic switch is mediated by the formation of a Gal4p-Gal80p-Gal3p complex. EMBO J. 17 (1998), 4086–4091.
32. Pilauri, V., Bewley, M., Diep, C., Hopper, J., Gal80 dimerization and the yeast GAL gene switch. Genetics 169 (2005), 1903–1914.
33. Maier, A., Völker, B., Boles, E., Fuhrmann, G.F., Characterisation of glucose transport in Saccharomyces cerevisiae with plasma membrane vesicles (countertransport) and intact cells (initial uptake) with single Hxt1, Hxt2, Hxt3, Hxt4, Hxt6, Hxt7 or Gal2 transporters. FEMS Yeast Res. 2 (2002), 539–550.
34. Mumma, J.O., Chhay, J.S., Ross, K.L., Eaton, J.S., Newell-Litwa, K.A., Fridovich-Keil, J.L., Distinct roles of galactose-1P in galactose-mediated growth arrest of yeast deficient in galactose-1P uridylyltransferase (GALT) and UDP-galactose 4′-epimerase (GALE). Mol. Genet. Metab. 93 (2008), 160–171.
35. Ross, K.L., Davis, C.N., Fridovich-Keil, J.L., Differential roles of the Leloir pathway enzymes and metabolites in defining galactose sensitivity in yeast. Mol. Genet. Metab. 83 (2004), 103–116.
36. Machado, C.M., De-Souza, E.A., De-Queiroz, A.L.F.V., Pimentel, F.S.A., Silva, G.F.S., Gomes, F.M., Montero-Lomelí M., Masuda, C.A., The galactose-induced decrease in phosphate levels leads to toxicity in yeast models of galactosemia. Biochim. Biophys. Acta. Mol. Basis. Dis. 1863 (2017), 1403–1409.
37. Marshall, V.M.E., Tamime, A.Y., Microbiology and technology of fermented milks. Law, B.A., (eds.) Microbiology and Biochemistry of Cheese and Fermented Milk, 1997, Blackie Academic & Professional, 57–152.
38. Bai, M., Qing, M., Guo, Z., Zhang, Y., Chen, X., Bao, Q., Zhang, H., Sun, T.S., Occurrence and dominance of yeast species in naturally fermented milk from the Tibetan Plateau of China. Can. J. Microbiol. 56 (2010), 707–714.
39. Hittinger, C.T., Carroll, S.B., Gene duplication and the adaptive evolution of a classic genetic switch. Nature 449 (2007), 677–681.
40. Hittinger, C.T., Gonçalves, P., Sampaio, J.P., Dover, J., Johnston, M., Rokas, A., Remarkably ancient balanced polymorphisms in a multi-locus gene network. Nature 464 (2010), 54–58.
41. Hittinger, C.T., Rokas, A., Carroll, S.B., Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts. Proc. Natl. Acad. Sci. USA 101 (2004), 14144–14149.
42. Kuang, M.C., Hutchins, P.D., Russell, J.D., Coon, J.J., Hittinger, C.T., Ongoing resolution of duplicate gene functions shapes the diversification of a metabolic network. eLife, 5, 2016, e19027.
43. Roop, J.I., Chang, K.C., Brem, R.B., Polygenic evolution of a sugar specialization trade-off in yeast. Nature 530 (2016), 336–339.
44. Breunig, K.D., Multicopy plasmids containing the gene for the transcriptional activator LAC9 are not tolerated by K. lactis cells. Curr. Genet. 15 (1989), 143–148.
45. Rubio-Texeira, M., A comparative analysis of the GAL genetic switch between not-so-distant cousins: Saccharomyces cerevisiae versus Kluyveromyces lactis. FEMS Yeast Res. 5 (2005), 1115–1128.
46. Nelissen, B., De Wachter, R., Goffeau, A., Classification of all putative permeases and other membrane plurispanners of the major facilitator superfamily encoded by the complete genome of Saccharomyces cerevisiae. FEMS Microbiol. Rev. 21 (1997), 113–134.
47. Kasahara, T., Kasahara, M., Three aromatic amino acid residues critical for galactose transport in yeast Gal2 transporter. J. Biol. Chem. 275 (2000), 4422–4428.
48. Ramos, J., Szkutnicka, K., Cirillo, V.P., Characteristics of galactose transport in Saccharomyces cerevisiae cells and reconstituted lipid vesicles. J. Bacteriol. 171 (1989), 3539–3544.
49. Ostergaard, S., Olsson, L., Johnston, M., Nielsen, J., Increasing galactose consumption by Saccharomyces cerevisiae through metabolic engineering of the GAL gene regulatory network. Nat. Biotechnol. 18 (2000), 1283–1286.
50. Katoh, K., Standley, D.M., MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30 (2013), 772–780.
51. Stamatakis, A., RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30 (2014), 1312–1313.
52. Posada, D., jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25 (2008), 1253–1256.
53. Hutter, S., Vilella, A.J., Rozas, J., Genome-wide DNA polymorphism analyses using VariScan. BMC Bioinformatics 7 (2006), 409–418.
54. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., Salzberg, S.L., TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14 (2013), R36–R48.
55. Liao, Y., Smyth, G.K., Shi, W., featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30 (2014), 923–930.
56. Anders, S., Huber, W., Differential expression analysis for sequence count data. Genome Biol. 11 (2010), R106–R117.
57. Langfelder, P., Horvath, S., WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9 (2008), 559–571.
58. Haas, B.J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P.D., Bowden, J., Couger, M.B., Eccles, D., Li, B., Lieber, M., et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8 (2013), 1494–1512.
59. Wang, Q.M., Liu, W.Q., Liti, G., Wang, S.A., Bai, F.Y., Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity. Mol. Ecol. 21 (2012), 5404–5417.
60. Xu, H., Dong, X., Ai, Q., Mai, K., Xu, W., Zhang, Y., Zuo, R., Regulation of tissue LC-PUFA contents, Δ6 fatty acyl desaturase (FADS2) gene expression and the methylation of the putative FADS2 gene promoter by different dietary fatty acid profiles in Japanese seabass (Lateolabrax japonicus). PLoS ONE, 9, 2014, e87726.
61. Warringer, J., Blomberg, A., Automated screening in environmental arrays allows analysis of quantitative phenotypic profiles in Saccharomyces cerevisiae. Yeast 20 (2003), 53–67.
62. Warringer, J., Anevski, D., Liu, B., Blomberg, A., Chemogenetic fingerprinting by analysis of cellular growth dynamics. BMC Chem. Biol. 8 (2008), 3–12.
63. Warringer, J., Zörgö E., Cubillos, F.A., Zia, A., Gjuvsland, A., Simpson, J.T., Forsmark, A., Durbin, R., Omholt, S.W., Louis, E.J., et al. Trait variation in yeast is defined by population history. PLoS Genet., 7, 2011, e1002111.
64. Nair, N.U., Zhao, H., Mutagenic inverted repeat assisted genome engineering (MIRAGE). Nucleic Acids Res., 37, 2009, e9.
65. Meilhoc, E., Masson, J.M., Teissié J., High efficiency transformation of intact yeast cells by electric field pulses. Biotechnology (N. Y.) 8 (1990), 223–227.
66. Xie, J., Tao, L., Nobile, C.J., Tong, Y., Guan, G., Sun, Y., Cao, C., Hernday, A.D., Johnson, A.D., Zhang, L., et al. White-opaque switching in natural MTLa/α isolates of Candida albicans: evolutionary implications for roles in host adaptation, pathogenesis, and sex. PLoS Biol., 11, 2013, e1001525.
67. Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (2001), 402–408.