Insights into molecular evolution from yeast genomics

Yeast

Volumn 31, Issue 7, 2014, Pages 233-241

  Zarin, Taraneh ^a   Moses, Alan M ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Comparative genomics; Complex phenotypes; Experimental evolution; Functional genomics; Functional synthesis; Gene duplication; Gene order; Molecular evolution; Population genomics; Regulatory evolution

Indexed keywords

ARTICLE; FUNCTIONAL GENOMICS; FUNGAL GENETICS; FUNGAL GENOME; GENE CONTROL; GENE DUPLICATION; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; GENE ORDER; GENE REGULATORY NETWORK; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOMICS; MOLECULAR EVOLUTION; NATURAL SELECTION; NONHUMAN; PHENOTYPE; POPULATION STRUCTURE; PRIORITY JOURNAL; PROTEIN FUNCTION; QUANTITATIVE TRAIT LOCUS MAPPING; STATISTICAL ANALYSIS; SYSTEMS BIOLOGY; YEAST; GENETICS; PHYLOGENY; SACCHAROMYCES CEREVISIAE;

EVOLUTION, MOLECULAR; GENE DUPLICATION; GENETIC VARIATION; GENOME, FUNGAL; PHYLOGENY; SACCHAROMYCES CEREVISIAE;

EID: 84903878652     PISSN: 0749503X     EISSN: 10970061     Source Type: Journal    
DOI: 10.1002/yea.3018     Document Type: Article

References (125)

1. Albert FW, Treusch S, Shockley AH, et al. 2014. Genetics of single-cell protein abundance in large yeast populations. Nature 506(7489): 494-497.
2. Amoutzias GD, He Y, Gordon J, et al. 2010. Posttranslational regulation impacts the fate of duplicated genes. Proc Natl Acad Sci U S A 107(7): 2967-2971.
3. Aparicio S, Chapman J, Stupka E, et al. 2002. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297(5585): 1301-1310.
4. Baker CR, Booth LN, Sorrells TR, Johnson AD. 2012. Protein modularity, cooperative binding, and hybrid regulatory states underlie transcriptional network diversification. Cell 151(1): 80-95.
5. Baker CR, Hanson-Smith V, Johnson AD. 2013. Following gene duplication, paralog interference constrains transcriptional circuit evolution. Science (NY) 342(6154): 104-108.
6. Baker CR, Tuch BB, Johnson AD. 2011. Extensive DNA-binding specificity divergence of a conserved transcription regulator. Proc Natl Acad Sci U S A 108(18): 7493-7498.
7. Beltrao P, Bork P, Krogan NJ, van Noort V. 2013. Evolution and functional cross-talk of protein post-translational modifications. Mol Syst Biol 9(1): 714.
8. Beltrao P, Trinidad JC, Fiedler D, et al. 2009. Evolution of phosphoregulation: comparison of phosphorylation patterns across yeast species. PLoS Biol 7(6): e1000134.
9. Booth LN, Tuch BB, Johnson AD. 2010. Intercalation of a new tier of transcription regulation into an ancient circuit. Nature 468(7326): 959-963.
10. Botstein D, Fink GR. 2011. Yeast: an experimental organism for 21st century biology. Genetics 189(3): 695-704.
11. Brem RB, Yvert G, Clinton R, Kruglyak L. 2002. Genetic dissection of transcriptional regulation in budding yeast. Science (NY) 296(5568): 752-755.
12. Breslow DK, Cameron DM, Collins SR, et al. 2008. A comprehensive strategy enabling high-resolution functional analysis of the yeast genome. Nat Methods 5(8): 711-718.
13. Buckling A, Craig Maclean R, Brockhurst MA, Colegrave N. 2009. The Beagle in a bottle. Nature 457(7231): 824-829.
14. Bullard JH, Mostovoy Y, Dudoit S, Brem RB. 2010. Polygenic and directional regulatory evolution across pathways in Saccharomyces. Proc Natl Acad Sci U S A 107(11): 5058-5063.
15. Caudron F, Barral Y. 2013. A super-assembly of Whi3 encodes memory of deceptive encounters by single cells during yeast courtship. Cell 155(6): 1244-1257.
16. Celiker H, Gore J. 2013. Cellular cooperation: insights from microbes. Trends Cell Biol 23(1): 9-15.
17. Choi SS, Hannenhalli S. 2013. Three independent determinants of protein evolutionary rate. J Mol Evol 76(3): 98-111.
18. Cliften PF, Hillier LW, Fulton L, et al. 2001. Surveying Saccharomyces genomes to identify functional elements by comparative DNA sequence analysis. Genome Res 11(7): 1175-1186.
19. Cliften P, Sudarsanam P, Desikan A, et al. 2003. Finding functional features in Saccharomyces genomes by phylogenetic footprinting. Science 301(5629): 71-76.
20. Connelly CF, Akey JM. 2012. On the prospects of whole-genome association mapping in Saccharomyces cerevisiae. Genetics 191(4): 1345-1353.
21. Cutter AD, Moses AM. 2011. Polymorphism, divergence, and the role of recombination in Saccharomyces cerevisiae genome evolution. Mol Biol Evol 28(5): 1745-1754.
22. Dean AM, Thornton JW. 2007. Mechanistic approaches to the study of evolution: the functional synthesis. Nat Rev Genet 8(9): 675-688.
23. Diao L, Chen KC. 2012. Local ancestry corrects for population structure in Saccharomyces cerevisiae genome-wide association studies. Genetics 192(4): 1503-1511.
24. Dhar R, Sägesser R, Weikert C, Wagner A. 2013. Yeast adapts to a changing stressful environment by evolving cross-protection and anticipatory gene regulation. Mol Biol Evol 30(3): 573-588.
25. Doniger SW, Kim HS, Swain D, et al. 2008. A catalog of neutral and deleterious polymorphism in yeast. PLoS Genet 4(8): e1000183.
26. Drummond DA, Bloom JD, Adami C, et al. 2005. Why highly expressed proteins evolve slowly. Proc Natl Acad Sci U S A 102(40): 14338-14343.
27. Dujon B, Sherman D, Fischer G, et al. 2004. Genome evolution in yeasts. Nature 430(6995): 35-44.
28. Fay JC. 2013. The molecular basis of phenotypic variation in yeast. Curr Opin Genet Dev 23(6): 672-677.
29. Fraser HB, Hirsh AE, Steinmetz LM, et al. 2002. Evolutionary rate in the protein interaction network. Science 296(5568): 750-752.
30. Fraser HB, Levy S, Chavan A, et al. 2012. Polygenic cis-regulatory adaptation in the evolution of yeast pathogenicity. Genome Res 22(10): 1930-1939.
31. Fraser HB, Moses AM, Schadt EE. 2010. Evidence for widespread adaptive evolution of gene expression in budding yeast. Proc Natl Acad Sci U S A 107(7): 2977-2982.
32. Freschi L, Courcelles M, Thibault P, et al. 2011. Phosphorylation network rewiring by gene duplication. Mol Syst Biol 7(504): 504.
33. Galagan JE, Henn MR, Ma LJ, et al. 2005. Genomics of the fungal kingdom: insights into eukaryotic biology. Genome Res 15(12): 1620-1631.
34. Gasch AP, Moses AM, Chiang DY, et al. 2004. Conservation and evolution of cis-regulatory systems in ascomycete fungi. PLoS Biol 2(12): e398.
35. Geiler-Samerotte KA, Dion MF, Budnik BA, et al. 2011. Misfolded proteins impose a dosage-dependent fitness cost and trigger a cytosolic unfolded protein response in yeast. Proc Natl Acad Sci U S A 108(2): 680-685.
36. Giaever G, Chu AM, Ni L, et al. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418(6896): 387-391.
37. Goddard MR, Godfray HC, Burt A. 2005. Sex increases the efficacy of natural selection in experimental yeast populations. Nature 434(B11): 636-640.
38. Goffeau A, Barrell BG, Bussey H, et al. 1996. Life with 6000 genes. Science (NY) 274(5287): 546, 563-546, 567.
39. Gresham D, Desai MM, Tucker CM, et al. 2008. The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet 4(12): e1000303.
40. He X, Zhang J. 2005. Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169(2): 1157-1164.
41. Hietpas RT, Bank C, Jensen JD, Bolon DNA. 2013. Shifting fitness landscapes in response to altered environments: evolution. Int J Org Evol 67(12): 3512-3522.
42. Hietpas RT, Jensen JD, Bolon DNA. 2011. Experimental illumination of a fitness landscape. Proc Natl Acad Sci U S A 108(19): 7896-7901.
43. Hill JA, Otto SP. 2007. The role of pleiotropy in the maintenance of sex in yeast. Genetics 175(3): 1419-1427.
44. Hittinger CT. 2013. Saccharomyces diversity and evolution: a budding model genus. Trends Genet 29(5): 309-317.
45. Hittinger CT, Carroll SB. 2007. Gene duplication and the adaptive evolution of a classic genetic switch. Nature 449(7163): 677-681.
46. Hittinger CT, Gonçalves P, Sampaio JP, et al. 2010. Remarkably ancient balanced polymorphisms in a multi-locus gene network. Nature 464(7285): 54-58.
47. Hittinger CT, Rokas A, Carroll SB. 2004. Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts. Proc Natl Acad Sci U S A 101(39): 14144-14149.
48. Holt LJ, Tuch BB, Villén J, et al. 2009. Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science (NY) 325(5948): 1682-1686.
49. Hughes AL. 2005. Gene duplication and the origin of novel proteins. Proc Natl Acad Sci U S A 102(25): 8791-8792.
50. Hurst LD, Pál C, Lercher MJ. 2004. The evolutionary dynamics of eukaryotic gene order. Nat Rev Genet 5(4): 299-310.
51. Hurst LD, Williams EJB, Pál C. 2002. Natural selection promotes the conservation of linkage of co-expressed genes. Trends Genet 18(12): 604-606. http://www.ncbi.nlm.nih.gov/pubmed/12446137 [accessed on 25 February 2014].
52. Josephides C, Moses AM. 2011. Modeling the evolution of a classic genetic switch. BMC Syst Biol 5: 24.
53. Kellis M, Patterson N, Endrizzi M, et al. 2003. Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423(6937): 241-254.
54. Kimura M, Ohta T. 1974. On some principles governing molecular evolution. Proc Natl Acad Sci U S A 71(7): 2848-2852. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=388569andtool=pmcentrezandrendertype=abstract [accessed on 25 February 2014].
55. Kim PM, Lu LJ, Xia Y, Gerstein MB. 2006. Relating three-dimensional structures to protein networks provides evolutionary insights. Science (NY) 314(5807): 1938-1941.
56. Kirst ME, Scott J, Kirst M, et al. 2004. Coordinated genetic regulation of growth and lignin revealed by quantitative trait locus analysis of cDNA microarray data in an interspecific backcross of Eucalyptus. Plant Physiol 135(4): 2368-2378.
57. Koschwanez JH, Foster KR, Murray AW. 2011. Sucrose utilization in budding yeast as a model for the origin of undifferentiated multicellularity. PLoS Biol 9: e1001122.
58. Koschwanez JH, Foster KR, Murray AW. 2013. Improved use of a public good selects for the evolution of undifferentiated multicellularity. eLife 2, e00367.
59. Kuo D, Licon K, Bandyopadhyay S, et al. 2010. Coevolution within a transcriptional network by compensatory trans and cis mutations. Genome Res 20(12): 1672-1678.
60. Kvitek DJ, Sherlock G. 2013. Whole genome, whole population sequencing reveals that loss of signaling networks is the major adaptive strategy in a constant environment. PLoS Genet 9(11): e1003972.
61. Lesecque Y, Mouchiroud D, Duret L. 2013. GC-biased gene conversion in yeast is specifically associated with crossovers: molecular mechanisms and evolutionary significance. Mol Biol Evol 30(6): 1409-1419.
62. Landry CR, Townsend JP, Hartl DL, Cavalieri D. 2006. Ecological and evolutionary genomics of Saccharomyces cerevisiae. Mol Ecol 15(3): 575-591.
63. Lang GI, Botstein D. 2011. A test of the coordinated expression hypothesis for the origin and maintenance of the GAL cluster in yeast. PLoS One 6(9): e25290.
64. Lang GI, Rice DP, Hickman MJ, et al. 2013. Pervasive genetic hitchhiking and clonal interference in 40 evolving yeast populations. Nature 500(7464): 571-574.
65. Lavoie H, Hogues H, Mallick J, et al. 2010. Evolutionary tinkering with conserved components of a transcriptional regulatory network. PLoS Biol 8(3): e1000329.
66. Levine M, Tjian R. 2003. Transcription regulation and animal diversity. Nature 424(6945): 147-151.
67. Li H, Johnson AD. 2010. Evolution of transcription networks - lessons from yeasts. Curr Biol 20(17): R746-R753.
68. Liti G, Schacherer J. 2011. The rise of yeast population genomics. C R Biol 334(8-9): 612-619.
69. Liti G, Carter DM, Moses AM, et al. 2009. Population genomics of domestic and wild yeasts. Nature 458(7236): 337-341.
70. MacLean RC, Gudelj I. 2006. Resource competition and social conflict in experimental populations of yeast. Nature 441(7092): 498-501 [10.1038/nature04624].
71. Maere S, Bodt SD, Raes J, et al. 2005. Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci U S A 102(15): 5454-5459.
72. Mallick J, Whiteway M. 2013. The evolutionary rewiring of the ribosomal protein transcription pathway modifies the interaction of transcription factor heteromer Ifh1-Fhl1 (interacts with forkhead 1-forkhead-like 1) with the DNA-binding specificity element. J Biol Chem 288(24): 17508-17519. doi:10.1074/jbc.M112.436683
73. Marques AC, Vinckenbosch N, Brawand D, et al. 2008. Functional diversification of duplicate genes through subcellular adaptation of encoded proteins. Genome Biol 9(3): R54.
74. Martin HC, Roop JI, Schraiber JG, et al. 2012. Evolution of a membrane protein regulon in Saccharomyces. Mol Biol Evol 29(7): 1747-1756.
75. Martchenko M, Levitin A, Hogues H, et al. 2007. Transcriptional rewiring of fungal galactose-metabolism circuitry. Curr Biol 17(12): 1007-1013.
76. McGary KL, Slot JC, Rokas A. 2013. Physical linkage of metabolic genes in fungi is an adaptation against the accumulation of toxic intermediate compounds. Proc Natl Acad Sci U S A 110(28): 11481-11486.
77. Monks SA, Leonardson A, Zhu H, et al. 2004. Genetic inheritance of gene expression in human cell lines. Am J Hum Genet 75(6): 1094-1105.
78. Moses AM, Landry CR. 2010. Moving from transcriptional to phospho-evolution: generalizing regulatory evolution? Trends Genet 26(11): 462-467.
79. Nguyen Ba AN, Moses AM. 2010. Evolution of characterized phosphorylation sites in budding yeast. Mol Biol Evol 27(9): 2027-2037.
80. Nguyen Ba AN, Yeh BJ, van Dyk D, et al. 2012. Proteome-wide discovery of evolutionary conserved sequences in disordered regions. Sci Signal 5(215): rs1.
81. Oud B, Guadalupe-Medina V, Nijkamp JF, et al. 2013. Genome duplication and mutations in ACE2 cause multicellular, fast-sedimenting phenotypes in evolved Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 110(45): E4223-E4231.
82. Pál C, Hurst LD. 2003. Evidence for co-evolution of gene order and recombination rate. Nat Genet 33(3): 392-395.
83. Pál C, Papp B, Hurst LD. 2001. Highly expressed genes in yeast evolve slowly. Genetics 158(2): 927-931.
84. Pannala VR, Ahammed Sherief KY, et al. 2011. Dynamic analysis of the KlGAL regulatory system in Kluyveromyces lactis: a comparative study with Saccharomyces cerevisiae. Syst Synth Biol 5(1-2): 69-85.
85. Park C, Chen X, Yang J, Zhang J. 2013. Differential requirements for mRNA folding partially explain why highly expressed proteins evolve slowly. Proc Natl Acad Sci U S A 110(8): E678-E686.
86. Park S, Lehner B. 2013. Epigenetic epistatic interactions constrain the evolution of gene expression. Mol Syst Biol 9: 645.
87. Parts L. 2014. Genome-wide mapping of cellular traits in yeast. Yeast. doi:10.1002/yea.3010
88. 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(7): 1131-1138.
89. Presser A, Elowitz MB, Kellis M, Kishony R. 2008. The evolutionary dynamics of the Saccharomyces cerevisiae protein interaction network after duplication. Proc Natl Acad Sci U S A 105(3): 950-954.
90. Prud'homme B, Gompel N, Carroll SB. 2007. Emerging principles of regulatory evolution. Proc Natl Acad Sci U S A 104(suppl 1): 8605-8612.
91. Qian W, He X, Chan E, et al. 2011. Measuring the evolutionary rate of protein-protein interaction. Proc Natl Acad Sci U S A 108(21): 8725-8730.
92. Qian W, Ma D, Xiao C, et al. 2012a. The genomic landscape and evolutionary resolution of antagonistic pleiotropy in yeast. Cell Rep 2(5): 1399-1410.
93. Qian W, Yang JR, Pearson NM, et al. 2012b. Balanced codon usage optimizes eukaryotic translational efficiency. PLoS Genet 8(3): e1002603.
94. Qian W, Zhang J. 2009. Protein subcellular relocalization in the evolution of yeast singleton and duplicate genes. Genome Biol Evol 1: 198-204.
95. Ratcliff WC, Denison RF, Borrello M, Travisano M. 2012. Experimental evolution of multicellularity. Proc Natl Acad Sci U S A 109(5): 1595-1600.
96. Rokas A, Williams BL, King N, et al. 2003. Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425(6960): 798-804.
97. Ruderfer DM, Pratt SC, Seidel HS, Kruglyak L. 2006. Population genomic analysis of outcrossing and recombination in yeast. Nat Genet 38: 1077-1081.
98. Scannell DR, Wolfe KH. 2008. A burst of protein sequence evolution and a prolonged period of asymmetric evolution follow gene duplication in yeast. Genome Res 18(1): 137-147.
99. Scannell DR, Byrne KP, Gordon JL, et al. 2006. Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts. Nature 440(7082): 341-345.
100. Scannell DR, Frank AC, Conant GC, et al. 2007. Independent sorting-out of thousands of duplicated gene pairs in two yeast species descended from a whole-genome duplication. Proc Natl Acad Sci U S A 104(20): 8397-8402.
101. Scannell DR, Zill OA, Rokas A, et al. 2011. The awesome power of yeast evolutionary genetics: new genome sequences and strain resources for the Saccharomyces sensu stricto genus. G3 (Bethesda, MD) 1(1): 11-25.
102. Schacherer J, Shapiro JA, Ruderfer DM, Kruglyak L. 2009. Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458(7236): 342-345.
103. Schadt EE, Monks SA, Drake TA, et al. 2003. Genetics of gene expression surveyed in maize, mouse and man. Nature 205: 1-6.
104. Seoighe C, Wolfe KH. 1999. Yeast genome evolution in the post-genome era. Curr Opin Microbiol 2(5): 548-554.
105. Shou W, Ram S, Vilar JMG. 2007. Synthetic cooperation in engineered yeast populations. Proc Natl Acad Sci U S A 104(6): 1877-1882.
106. Slot JC, Rokas A. 2010. Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi. Proc Natl Acad Sci U S A 107(22): 10137-10141.
107. Smukalla S, Caldara M, Pochet N, et al. 2008. FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast. Cell 135(4): 726-737.
108. Soria PS, McGary KL, Rokas A. 2014. Functional divergence for every paralog. Mol Biol Evol 31(4): 984-992.
109. Sun MGF, Sikora M, Costanzo M, et al. 2012. Network evolution: rewiring and signatures of conservation in signaling. PLoS Comput Biol 8(3): e1002411.
110. Tirosh I, Barkai N. 2007. Comparative analysis indicates regulatory neofunctionalization of yeast duplicates. Genome Biol 8(4): R50.
111. Tirosh I, Reikhav S, Levy AA, Barkai N. 2009. A yeast hybrid provides insight into the evolution of gene expression regulation. Science (NY) 324(5927): 659-662.
112. Tirosh I, Sigal N, Barkai N. 2010. Divergence of nucleosome positioning between two closely related yeast species: genetic basis and functional consequences. Mol Syst Biol 6(365): 365.
113. Van Dyken JD, Müller MJI, Mack KML, Desai MM. 2013. Spatial population expansion promotes the evolution of cooperation in an experimental Prisoner's Dilemma. Curr Biol 23(10): 919-923.
114. Voordeckers K, Brown CA, Vanneste K, et al. 2012. Reconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication. PLoS Biol 10(12): e1001446.
115. Wang Z, Zhang J. 2009. Why is the correlation between gene importance and gene evolutionary rate so weak? PLoS Genet 5(1): e1000329.
116. Waterston RH, Lindblad-Toh K, Birney E, et al. 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420(6915): 520-562.
117. Weirauch MT, Hughes TR. 2010. Dramatic changes in transcription factor binding over evolutionary time. Genome Biol 11(6): 122.
118. Wohlbach DJ, Thompson DA, Gasch AP, Regev A. 2009. From elements to modules: regulatory evolution in Ascomycota fungi. Curr Opin Genet Dev 19(6): 571-578.
119. Wolfe KH. 2006. Comparative genomics and genome evolution in yeasts. Philos Trans R Soc Lond B Biol Sci 361(1467): 403-412.
120. Wolfe KH, Li WH. 2003. Molecular evolution meets the genomics revolution. Nat Genet 33: 255-265.
121. Wolfe KH, Shields DC. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387(6634): 708-713.
122. Wong S, Wolfe KH. 2005. Birth of a metabolic gene cluster in yeast by adaptive gene relocation. Nat Genet 37(7): 777-782.
123. Wray GA, Hahn MW, Abouheif E, et al. 2003. The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol 20(9): 1377-1419.
124. Yang JR, Liao BY, Zhuang SM, Zhang J. 2012. Protein misinteraction avoidance causes highly expressed proteins to evolve slowly. Proc Natl Acad Sci U S A 109(14): E831-E840.
125. Zheng W, Zhao H, Mancera E, et al. 2010. Genetic analysis of variation in transcription factor binding in yeast. Nature 464(7292): 1187-1191. http://dx.doi.org/10.1038/nature08934 [accessed on 25 February 2014].