The evolution of gene expression regulatory networks in yeasts (original) (raw)

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Comparative genomics sheds light on the evolution of gene expression regulatory networks across yeast species. Utilizing recent advancements in transcriptomics, this article reviews the significant genomic changes and diversity among approximately 20 yeast species sequenced via the Genolevures program, revealing how variations in cisregulatory elements and transregulatory proteins can lead to substantial rewiring of regulatory interactions. This insight into the evolutionary dynamics of gene regulation contributes to the emerging field of comparative functional genomics.

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References (74)

  1. I. Wapinski, A. Pfeffer, N. Friedman, A. Regev, Natural history and evolutionary principles of gene duplication in fungi, Nature 449 (2007) 54-61.
  2. J.L. Souciet, et al., Comparative genomics of protoploid Saccharomyce- taceae, Genome Res. 19 (2009) 1696-1709.
  3. L.J. Ma, et al., Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium, Nature 464 (2010) 367-373.
  4. G. Fischer, E.P. Rocha, F. Brunet, M. Vergassola, B. Dujon, Highly variable rates of genome rearrangements between hemiascomycetous yeast lineages, PLoS Genet. 2 (2006) e32.
  5. I. Wapinski, A. Regev, Reconstructing gene histories in Ascomycota fungi, Methods Enzymol. 470 (2010) 447-485.
  6. A. Mazurie, S. Bottani, M. Vergassola, An evolutionary and functional assessment of regulatory network motifs, Genome Biol. 6 (2005) R35.
  7. A.P. Gasch, A.M. Moses, D.Y. Chiang, H.B. Fraser, M. Berardini, M.B. Eisen, Conservation and evolution of cis-regulatory systems in asco- mycete fungi, PLoS Biol. 2 (2004) e398.
  8. M. Kellis, N. Patterson, M. Endrizzi, B. Birren, E.S. Lander, Sequencing and comparison of yeast species to identify genes and regulatory elements, Nature 423 (2003) 241-254.
  9. I. Tirosh, Y. Bilu, N. Barkai, Comparative biology: beyond sequence analysis, Curr. Opin. Biotechnol. 18 (2007) 371-377.
  10. D.J. Wohlbach, D.A. Thompson, A.P. Gasch, A. Regev, From elements to modules: regulatory evolution in Ascomycota fungi, Curr. Opin. Genet. Dev. 19 (2009) 571-578.
  11. B. Dujon, Hemiascomycetous yeasts at the forefront of comparative genomics, Curr. Opin. Genet. Dev. 15 (2005) 614-620.
  12. I. Wapinski, J. Pfiffner, C. French, A. Socha, D.A. Thompson, A. Regev, Gene duplication and the evolution of ribosomal protein gene regula- tion in yeast, Proc. Natl. Acad. Sci. U S A 107 (2010) 5505-5510.
  13. A. Roetzer, et al., Candida glabrata environmental stress response involves Saccharomyces cerevisiae Msn2/4 orthologous transcription factors, Mol. Microbiol. 69 (2008) 603-620.
  14. J. Ihmels, S. Bergmann, M. Gerami-Nejad, I. Yanai, M. McClellan, J. Berman, N. Barkai, Rewiring of the yeast transcriptional network through the evolution of motif usage, Science 309 (2005) 938-940.
  15. I. Tirosh, A. Weinberger, D. Bezalel, M. Kaganovich, N. Barkai, On the relation between promoter divergence and gene expression evolution, Mol. Syst. Biol. 4 (2008) 159.
  16. J. Ihmels, S. Bergmann, J. Berman, N. Barkai, Comparative gene expres- sion analysis by differential clustering approach: application to the Candida albicans transcription program, PLoS Genet. 1 (2005) e39.
  17. G. Lelandais, V. Tanty, C. Geneix, C. Etchebest, C. Jacq, F. Devaux, Genome adaptation to chemical stress: clues from comparative tran- scriptomics in Saccharomyces cerevisiae and Candida glabrata, Genome Biol. 9 (2008) R164.
  18. D. Kuo, K. Tan, G. Zinman, T. Ravasi, Z. Bar-Joseph, T. Ideker, Evolution- ary divergence in the fungal response to fluconazole revealed by soft clustering, Genome Biol. 11 (2010) R77.
  19. J.L. DeRisi, V.R. Iyer, P.O. Brown, Exploring the metabolic and genetic control of gene expression on a genomic scale, Science 278 (1997) 680-686.
  20. A.P. Gasch, Comparative genomics of the environmental stress re- sponse in ascomycete fungi, Yeast 24 (2007) 961-976.
  21. O.R. Homann, J. Dea, S.M. Noble, A.D. Johnson, A phenotypic profile of the Candida albicans regulatory network, PLoS Genet. 5 (2009) e1000783.
  22. D. Kuo, et al., Coevolution within a transcriptional network by com- pensatory trans and cis mutations, Genome Res. 20 (2010) 1672-1678.
  23. A.R. Borneman, et al., Divergence of transcription factor binding sites across related yeast species, Science 317 (2007) 815-819.
  24. A.E. Tsong, B.B. Tuch, H. Li, A.D. Johnson, Evolution of alternative transcriptional circuits with identical logic, Nature 443 (2006) 415-420.
  25. B.B. Tuch, D.J. Galgoczy, A.D. Hernday, H. Li, A.D. Johnson, The evolution of combinatorial gene regulation in fungi, PLoS Biol. 6 (2008) e38.
  26. H. Lavoie, H. Hogues, J. Mallick, A. Sellam, A. Nantel, M. Whiteway, Evolutionary tinkering with conserved components of a transcriptional regulatory network, PLoS Biol. 8 (2010) e1000329.
  27. H. Hogues, H. Lavoie, A. Sellam, M. Mangos, T. Roemer, E. Purisima, A. Nantel, M. Whiteway, Transcription factor substitution during the evolution of fungal ribosome regulation, Mol. Cell. 29 (2008) 552-562.
  28. M. Martchenko, A. Levitin, H. Hogues, A. Nantel, M. Whiteway, Tran- scriptional rewiring of fungal galactose-metabolism circuitry, Curr. Biol. 17 (2007) 1007-1013.
  29. I. Tirosh, N. Barkai, Evolution of gene sequence and gene expression are not correlated in yeast, Trends Genet. 24 (2008) 109-113.
  30. S. Znaidi, K.S. Barker, S. Weber, A.M. Alarco, T.T. Liu, G. Boucher, P.D. Rogers, M. Raymond, Identification of the Candida albicans Cap1p regulon, Eukaryot Cell. 8 (2009) 806-820.
  31. I. Tirosh, N. Barkai, Two strategies for gene regulation by promoter nucleosomes, Genome Res. 18 (2008) 1084-1091.
  32. Y. Field, et al., Gene expression divergence in yeast is coupled to evolution of DNA-encoded nucleosome organization, Nat. Genet. 41 (2009) 438-445.
  33. I. Tirosh, N. Sigal, N. Barkai, Divergence of nucleosome positioning between two closely related yeast species: genetic basis and functional consequences, Mol. Syst. Biol. 6 (2010) 365.
  34. A.M. Tsankov, D.A. Thompson, A. Socha, A. Regev, O.J. Rando, The role of nucleosome positioning in the evolution of gene regulation, PLoS Biol. 8 (2010) e1000414.
  35. J.D. Keene, RNA regulons: coordination of post-transcriptional events, Nat. Rev. Genet. 8 (2007) 533-543.
  36. G. Lelandais, Y. Saint-Georges, C. Geneix, L. Al-Shikhley, G. Dujardin, C. Jacq, Spatio-temporal dynamics of yeast mitochondrial biogenesis: transcriptional and post-transcriptional mRNA oscillatory modules, PLoS Comput. Biol. 5 (2009) e1000409.
  37. B.C. Foat, S.S. Houshmandi, W.M. Olivas, H.J. Bussemaker, Profiling condition-specific, genome-wide regulation of mRNA stability in yeast, Proc. Natl. Acad. Sci. U S A 102 (2005) 17675-17680.
  38. D.J Hogan, D.P. Riordan, A.P. Gerber, D. Herschlag, P.O. Brown, Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system, PLoS Biol. 6 (2008) e255.
  39. H. Jiang, W. Guan, Z. Gu, Tinkering evolution of post-transcriptional RNA regulons: puf3p in fungi as an example, PLoS Genet. 6 (2010) e1001030.
  40. I.A. Drinnenberg, D.E. Weinberg, K.T. Xie, J.P. Mower, K.H. Wolfe, G.R. Fink, D.P. Bartel, RNAi in budding yeast, Science 326 (2009) 544-550.
  41. S.L. Bumgarner, R.D. Dowell, P. Grisafi, D.K. Gifford, G.R. Fink, Toggle involving cis-interfering noncoding RNAs controls variegated gene expression in yeast, Proc. Natl. Acad. Sci. U S A 106 (2009) 18321-18326.
  42. H. Neil, C. Malabat, Y. d'Aubenton-Carafa, Z. Xu, L.M. Steinmetz, A. Jacquier, Widespread bidirectional promoters are the major source of cryptic transcripts in yeast, Nature 457 (2009) 1038-1042.
  43. Z. Xu, et al., Bidirectional promoters generate pervasive transcription in yeast, Nature 457 (2009) 1033-1037.
  44. U. Nagalakshmi, Z. Wang, K. Waern, C. Shou, D. Raha, M. Gerstein, M. Snyder, The transcriptional landscape of the yeast genome defined by RNA sequencing, Science 320 (2008) 1344-1349.
  45. V.M. Bruno, Z. Wang, S.L. Marjani, G.M. Euskirchen, J. Martin, G. Sherlock, M. Snyder, Comprehensive annotation of the transcriptome of the human fungal pathogen Candida albicans using RNA-seq, Genome Res. 20 (2010) 1451-1458.
  46. A. Sellam, et al., Experimental annotation of the human pathogen Candida albicans coding and noncoding transcribed regions using high-resolution tiling arrays, Genome Biol. 11 (2010) R71.
  47. O.K. Yoon, R.B. Brem, Noncanonical transcript forms in yeast and their regulation during environmental stress, Rna 16 (2010) 1256-1267.
  48. M. Yassour, et al., Strand-specific RNA sequencing reveals extensive regulated long antisense transcripts that are conserved across yeast species, Genome Biol. 11 (2010) R87.
  49. J.H. Bullard, Y. Mostovoy, S. Dudoit, R.B. Brem, Polygenic and directional regulatory evolution across pathways in Saccharomyces, Proc. Natl. Acad. Sci. U S A 107 (2010) 5058-5063.
  50. I. Tirosh, S. Reikhav, A.A. Levy, N. Barkai, A yeast hybrid provides insight into the evolution of gene expression regulation, Science 324 (2009) 659-662.
  51. J. Schacherer, J.A. Shapiro, D.M. Ruderfer, L. Kruglyak, Comprehensive polymorphism survey elucidates population structure of Saccharomy- ces cerevisiae, Nature 458 (2009) 342-345.
  52. G. Liti, et al., Population genomics of domestic and wild yeasts, Nature 458 (2009) 337-341.
  53. D.J. Kvitek, J.L. Will, A.P. Gasch, Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolates, PLoS Genet. 4 (2008) e1000223.
  54. W. Zheng, H. Zhao, E. Mancera, L.M. Steinmetz, M. Snyder, Genetic analysis of variation in transcription factor binding in yeast, Nature 464 (2010) 1187-1191.
  55. R.B. Brem, G. Yvert, R. Clinton, L. Kruglyak, Genetic dissection of transcriptional regulation in budding yeast, Science 296 (2002) 752-755.
  56. G. Yvert, R.B. Brem, J. Whittle, J.M. Akey, E. Foss, E.N. Smith, R. Mack- elprang, L. Kruglyak, Trans-acting regulatory variation in Saccharomy- ces cerevisiae and the role of transcription factors, Nat. Genet. 35 (2003) 57-64.
  57. R.B. Brem, J.D. Storey, J. Whittle, L. Kruglyak, Genetic interactions between polymorphisms that affect gene expression in yeast, Nature 436 (2005) 701-703.
  58. R.B. Brem, L. Kruglyak, The landscape of genetic complexity across 5,700 gene expression traits in yeast, Proc. Natl. Acad. Sci. U S A 102 (2005) 1572-1757.
  59. C.L. Araya, C. Payen, M.J. Dunham, S. Fields, Whole-genome sequencing of a laboratory-evolved yeast strain, BMC Genomics 11 (2010) 88.
  60. D. Gresham, et al., The repertoire and dynamics of evolutionary adap- tations to controlled nutrient-limited environments in yeast, PLoS Genet. 4 (2008) e1000303.
  61. R. Koszul, S. Caburet, B. Dujon, G. Fischer, Eucaryotic genome evolution through the spontaneous duplication of large chromosomal segments, Embo J 23 (2004) 234-243.
  62. C. Payen, R. Koszul, B. Dujon, G. Fischer, Segmental duplications arise from Pol32-dependent repair of broken forks through two alternative replication-based mechanisms, PLoS Genet. 4 (2008) e1000175.
  63. E. Dekel, U. Alon, Optimality and evolutionary tuning of the expression level of a protein, Nature 436 (2005) 588-592.
  64. S. Stern, T. Dror, E. Stolovicki, N. Brenner, E. Braun, Genome-wide transcriptional plasticity underlies cellular adaptation to novel chal- lenge, Mol. Syst. Biol. 3 (2007) 106.
  65. A. Hintze, C. Adami, Evolution of complex modular biological networks, PLoS Comput. Biol. 4 (2008) e23.
  66. D. Fusco, L. Grassi, B. Bassetti, M. Caselle, M. Cosentino Lagomarsino, Ordered structure of the transcription network inherited from the yeast whole-genome duplication, BMC Syst. Biol. 4 (2010) 77.
  67. L. Grassi, D. Fusco, A. Sellerio, D. Cora, B. Bassetti, M. Caselle, M.C. Lagomarsino, Identity and divergence of protein domain architectures after the yeast whole-genome duplication event, Mol. Biosyst. 6 (2010) 2305-2315.
  68. M. Novo, et al., Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118, Proc. Natl. Acad. Sci. U S A 106 (2009) 16333-16338.
  69. T. Rolland, C. Neuveglise, C. Sacerdot, B. Dujon, Insertion of horizontally transferred genes within conserved syntenic regions of yeast genomes, PLoS One 4 (2009) e6515.
  70. J. Ihmels, S.R. Collins, M. Schuldiner, N.J. Krogan, J.S. Weissman, Backup without redundancy: genetic interactions reveal the cost of duplicate gene loss, Mol. Syst. Biol. 3 (2007) 86.
  71. C.T. Hittinger, S.B. Carroll, Gene duplication and the adaptive evolution of a classic genetic switch, Nature 449 (2007) 677-681.
  72. K. Tan, H. Feizi, C. Luo, S.H. Fan, T. Ravasi, T.G. Ideker, A systems approach to delineate functions of paralogous transcription factors: role of the Yap family in the DNA damage response, Proc. Natl. Acad. Sci. U S A 105 (2008) 2934-2939.
  73. A. Lucau-Danila, G. Lelandais, Z. Kozovska, V. Tanty, T. Delaveau, F. Devaux, C. Jacq, Early expression of yeast genes affected by chemical stress, Mol. Cell. Biol. 25 (2005) 1860-1868.
  74. H. Salin, V. Fardeau, E. Piccini, G. Lelandais, V. Tanty, S. Lemoine, C. Jacq, F. Devaux, Structure and properties of transcriptional networks driving selenite stress response in yeasts, BMC Genomics 9 (2008) 333.