Genomic insights into the different layers of gene regulation in yeast (original) (raw)

Abstract

The model organism Saccharomyces cerevisiae has allowed the development of new functional genomics techniques devoted to the study of transcription in all its stages. With these techniques, it has been possible to find interesting new mechanisms to control gene expression that act at different levels and for different gene sets apart from the known cis-trans regulation in the transcription initiation step. Here we discuss a method developed in our laboratory, Genomic Run-On, and other new methods that have recently appeared with distinct technical features. A comparison between the datasets generated by them provides interesting genomic insights into the different layers of gene regulation in eukaryotes.

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References (71)

  1. S. Brenner, "Detective Rummage investigates," The Scientist, vol. 16, no. 16, p. 15, 2002.
  2. M. Snyder and J. E. G. Gallagher, "Systems biology from a yeast omics perspective," FEBS Letters, vol. 583, no. 24, pp. 3895- 3899, 2009.
  3. J. Beckwith, "The operon as paradigm: normal science and the beginning of biological complexity," Journal Of Molecular Biology, vol. 409, no. 1, pp. 7-13, 2011.
  4. A. Goffeau, B. G. Barrell, H. Bussey et al., "Life with 6000 genes," Science, vol. 274, no. 5287, pp. 546-567, 1996.
  5. S. R. Engel, R. Balakrishnan, G. Binkley et al., "Saccharomyces genome database provides mutant phenotype data," Nucleic Acids Research, vol. 38, supplement1, pp. D433-D436, 2009.
  6. U. Güldener, M. Münsterkötter, G. Kastenmüller et al., "CYGD: the comprehensive yeast genome database," Nucleic Acids Research, vol. 33, supplement 1, pp. D364-D368, 2005.
  7. J. E. Pérez-Ortín, J. García-Martínez, and T. M. Alberola, "DNA chips for yeast biotechnology. The case of wine yeasts," Journal of Biotechnology, vol. 98, no. 2-3, pp. 227-241, 2002.
  8. J. L. DeRisi, V. R. Iyer, and P. O. Brown, "Exploring the metabolic and genetic control of gene expression on a genomic scale," Science, vol. 278, no. 5338, pp. 680-686, 1997.
  9. N. C. Hauser, M. Vingron, M. Scheideler et al., "Transcrip- tional profiling on all open reading frames of Saccharomyces cerevisiae," Yeast, vol. 14, no. 13, pp. 1209-1221, 1998.
  10. L. David, W. Huber, M. Granovskaia et al., "A high-resolution map of transcription in the yeast genome," Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 14, pp. 5320-5325, 2006.
  11. C. T. Harbison, D. B. Gordon, T. I. Lee et al., "Transcriptional regulatory code of a eukaryotic genome," Nature, vol. 430, no. 7004, pp. 99-104, 2004.
  12. S. Brenner, "Sequences and consequences," Philosophical Transactions of the Royal Society B, vol. 365, no. 1537, pp. 207- 212, 2010.
  13. F. Wyers, M. Rougemaille, G. Badis et al., "Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase," Cell, vol. 121, no. 5, pp. 725-737, 2005.
  14. Z. Xu, W. Wei, J. Gagneur et al., "Bidirectional promoters generate pervasive transcription in yeast," Nature, vol. 457, no. 7232, pp. 1033-1037, 2009.
  15. M. Yassour, J. Pfiffner, J. Z. Levin et al., "Strand-specific RNA sequencing reveals extensive regulated long antisense transcripts that are conserved across yeast species," Genome Biology, 2010, article R87.
  16. R. Parker and H. Song, "The enzymes and control of eukar- yotic mRNA turnover," Nature Structural and Molecular Biology, vol. 11, no. 2, pp. 121-127, 2004.
  17. Y. Wang, C. L. Liu, J. D. Storey, R. J. Tibshirani, D. Herschlag, and P. O. Brown, "Precision and functional specificity in mRNA decay," Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 9, pp. 5860-5865, 2002.
  18. R. Parker, D. Herrick, S. W. Peltz, and A. Jacobson, "Mea- surement of mRNA decay rates in Saccharomyces cerevisiae," Methods in Enzymology, vol. 194, pp. 415-423, 1991.
  19. J. Grigull, S. Mnaimneh, J. Pootoolal, M. D. Robinson, and T. R. Hughes, "Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttran- scriptional control of ribosome biogenesis factors," Molecular and Cellular Biology, vol. 24, no. 12, pp. 5534-5547, 2004.
  20. J. E. Pérez-Ortín, P. M. Alepuz, and J. Moreno, "Genomics and gene transcription kinetics in yeast," Trends in Genetics, vol. 23, no. 5, pp. 250-257, 2007.
  21. V. Pelechano and J. E. Pérez-Ortín, "There is a steady-state transcriptome in exponentially growing yeast cells," Yeast, vol. 27, no. 7, pp. 413-422, 2010.
  22. K. Hirayoshi and J. T. Lis, "Nuclear run-on assays: assessing transcription by measuring density of engaged RNA poly- merases," Methods in Enzymology, vol. 304, pp. 351-362, 1999.
  23. J. García-Martínez, A. Aranda, and J. E. Pérez-Ortín, "Genomic run-on evaluates transcription rates for all yeast genes and identifies gene regulatory mechanisms," Molecular Cell, vol. 15, no. 2, pp. 303-313, 2004.
  24. T. M. Alberola, J. García-Martínez, O. Ant únez et al., "A new set of DNA macrochips for the yeast Saccharomyces cerevisiae: features and uses," International Microbiology, vol. 7, no. 3, pp. 199-206, 2004.
  25. L. J. Core, J. J. Waterfall, and J. T. Lis, "Nascent RNA sequenc- ing reveals widespread pausing and divergent initiation at human promoters," Science, vol. 322, no. 5909, pp. 1845-1848, 2008.
  26. J. García-Martínez, V. Pelechano, and J. E. Pérez-Ortín, "Genomic-wide methods to evaluate transcription rates in yeast," Methods in Molecular Biology, vol. 734, pp. 25-44, 2011.
  27. M. M. Molina-Navarro, L. Castells-Roca, G. Bellí et al., "Com- prehensive transcriptional analysis of the oxidative response in yeast," Journal of Biological Chemistry, vol. 283, no. 26, pp. 17908-17918, 2008.
  28. L. Romero-Santacreu, J. Moreno, J. E. Pérez-Ortín, and P. Alepuz, "Specific and global regulation of mRNA stability during osmotic stress in Saccharomyces cerevisiae," RNA, vol. 15, no. 6, pp. 1110-1120, 2009.
  29. L. Castells-Roca, J. García-Martínez, J. Moreno, E. Herrero, G. Belli, and J. E. Perez-Ortin, "Heat shock response in yeast involves changes in both transcription rates and mRNA stabilities," PLoS One, vol. 6, Article ID e17272, 2011.
  30. B. Hayles, S. Yellaboina, and D. Wang, "Comparing transcrip- tion rate and mRNA abundance as parameters for biochemical pathway and network analysis," PLoS One, vol. 5, Article ID e9908, 2010.
  31. V. Pelechano, S. Chávez, and J. E. Pérez-Ortín, "A complete set of nascent transcription rates for yeast genes," PLoS One, vol. 5, no. 11, Article ID e15442, 2010.
  32. F. Carrillo-Oesterreich, S. Preibisch, and K. M. Neugebauer, "Global analysis of nascent rna reveals transcriptional pausing in terminal exons," Molecular Cell, vol. 40, no. 4, pp. 571-581, 2010.
  33. A. Mayer, M. Lidschreiber, M. Siebert, K. Leike, J. Söding, and P. Cramer, "Uniform transitions of the general RNA polymerase II transcription complex," Nature Structural and Molecular Biology, vol. 17, no. 10, pp. 1272-1278, 2010.
  34. V. Pelechano, S. Gimeno-González, A. Rodríguez-Gil, J. García-Martínez, J. E. Pérez-Ortín, and S. Chávez, "Regulon- specific control of transcription elongation across the yeast genome," PLoS Genetics, vol. 5, no. 8, Article ID e1000614, 2009.
  35. P. Lefrancois, G. M. Euskirchen, R. K. Auerbach et al., "Efficient yeast ChIP-Seq using multiplex short-read DNA sequencing," BMC Genomics, vol. 10, article 37, 2009.
  36. L. S. Churchman and J. S. Weissman, "Nascent transcript sequencing visualizes transcription at nucleotide resolution," Nature, vol. 469, pp. 368-373, 2011.
  37. C. Miller, B. Schwalb, K. Maier et al., "Dynamic transcriptome analysis measures rates of mRNA synthesis and decay in yeast," Molecular Systems Biology, vol. 7, article 458, 2011.
  38. J. Fan, X. Yang, W. Wang, W. H. Wood, K. G. Becker, and M. Gorospe, "Global analysis of stress-regulated mRNA turnover by using cDNA arrays," Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 16, pp. 10611-10616, 2002.
  39. J. García-Martínez, F. González-Candelas, and J. E. Pérez- Ortín, "Common gene expression strategies revealed by genome-wide analysis in yeast," Genome Biology, vol. 8, no. 10, article R222, 2007.
  40. K. Struhl, "Transcriptional noise and the fidelity of initiation by RNA polymerase II," Nature Structural and Molecular Biology, vol. 14, no. 2, pp. 103-105, 2007.
  41. A. Marín, M. Gallardo, Y. Kato et al., "Relationship between G+C content, ORF-length and mRNA concentration in Sac- charomyces cerevisiae," Yeast, vol. 20, no. 8, pp. 703-711, 2003.
  42. W. Wei, V. Pelechano, A. I. Järvelin, and L. M. Steinmetz, "Functional consequences of bidirectional promoters," Trends in Genetics, vol. 27, no. 7, pp. 267-276, 2011.
  43. T. S. Kim, C. L. Liu, M. Yassour et al., "RNA Polymerase mapping during stress responses reveals widespread nonpro- ductive transcription in yeast," Genome Biology, 2010, article R75.
  44. M. Rabani, J. Z. Levin, L. Fan et al., "Metabolic labeling of RNA uncovers principles of RNA production and degradation dynamics in mammalian cells," Nature Biotechnology, vol. 29, no. 5, pp. 436-442, 2011.
  45. E. M. Airoldi, C. Huttenhower, D. Gresham et al., "Predicting cellular growth from gene expression signatures," PLoS Com- putational Biology, vol. 5, no. 1, Article ID e1000257, 2009.
  46. M. Kenzelmann, S. Maertens, M. Hergenhahn et al., "Microar- ray analysis of newly synthesized RNA in cells and animals," Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 15, pp. 6164-6169, 2007.
  47. F. C. P. Holstege, E. G. Jennings, J. J. Wyrick et al., "Dissecting the regulatory circuitry of a eukaryotic genome," Cell, vol. 95, no. 5, pp. 717-728, 1998.
  48. J. R. Warner, "The economics of ribosome biosynthesis in yeast," Trends in Biochemical Sciences, vol. 24, no. 11, pp. 437- 440, 1999.
  49. M. C. Bosio, R. Negri, and G. Dieci, "Promoter architectures in the yeast ribosomal expression program," Transcription, vol. 2, no. 2, pp. 71-77, 2011.
  50. H. Lempiäinen and D. Shore, "Growth control and ribosome biogenesis," Current Opinion in Cell Biology, vol. 21, no. 6, pp. 855-863, 2009.
  51. D. Wang, D. A. Bushnell, X. Huang, K. D. Westover, M. Levitt, and R. D. Kornberg, "Structural basis of transcription: backtracked RNA Polymerase II at 3.4 angstrom Resolution," Science, vol. 324, no. 5931, pp. 1203-1206, 2009.
  52. I. R. Graham, R. A. Haw, K. G. Spink, K. A. Halden, and A. Chambers, "In vivo analysis of functional regions within yeast Rap1p," Molecular and Cellular Biology, vol. 19, no. 11, pp. 7481-7490, 1999.
  53. P. Jorgensen, I. Rupeš, J. R. Sharom, L. Schneper, J. R. Broach, and M. Tyers, "A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size," Genes and Development, vol. 18, no. 20, pp. 2491-2505, 2004.
  54. K. Fredrick and M. Ibba, "How the sequence of a gene can tune its translation," Cell, vol. 141, no. 2, pp. 227-229, 2010.
  55. A. N. Boettiger, P. L. Ralph, and S. N. Evans, "Transcriptional regulation: effects of promoter proximal pausing on speed, synchrony and reliability," PLoS Computational Biology, vol. 7, no. 5, Article ID e1001136, 2011.
  56. J. R. S. Newman, S. Ghaemmaghami, J. Ihmels et al., "Single- cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise," Nature, vol. 441, no. 7095, pp. 840-846, 2006.
  57. J. D. Keene, "RNA regulons: coordination of post-trans- criptional events," Nature Reviews Genetics, vol. 8, no. 7, pp. 533-543, 2007.
  58. A. P. Gerber, D. Herschlag, and P. O. Brown, "Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast," PLoS Biology, vol. 2, no. 3, article e79, 2004.
  59. D. J. Hogan, D. P. Riordan, A. P. Gerber, D. Herschlag, and P. O. Brown, "Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system," PLoS Biology, vol. 6, no. 10, article e255, 2008.
  60. S. A. Tenenbaum, C. C. Carson, U. Atasoy, and J. D. Keene, "Genome-wide regulatory analysis using en masse nuclear run-ons and ribonomic profiling with autoimmune sera," Gene, vol. 317, no. 1-2, pp. 79-87, 2003.
  61. O. Shalem, O. Dahan, M. Levo et al., "Transient transcriptional responses to stress are generated by opposing effects of mRNA production and degradation," Molecular Systems Biology, vol. 4, article 4, 2008.
  62. C. Molin, A. Jauhiainen, J. Warringer, O. Nerman, and P. E. R. Sunnerhagen, "mRNA stability changes precede changes in steady-state mRNA amounts during hyperosmotic stress," RNA, vol. 15, no. 4, pp. 600-614, 2009.
  63. M. Chatenay-Laponte and G. S. Shadel, "Repression of mitochondrial translation, respiration and a metabolic cycle- regulated gene, SLF1, by the yeast pumilio-family protein Puf3p," PLoS One, vol. 6, no. 5, Article ID e20441, 2011.
  64. A. P. Gasch, P. T. Spellman, C. M. Kao et al., "Genomic expres- sion programs in the response of yeast cells to environmental changes," Molecular Biology of the Cell, vol. 11, no. 12, pp. 4241-4257, 2000.
  65. D. Zenklusen, D. R. Larson, and R. H. Singer, "Single-RNA counting reveals alternative modes of gene expression in yeast," Nature Structural and Molecular Biology, vol. 15, no. 12, pp. 1263-1271, 2008.
  66. B. Schwanhäusser, D. Busse, N. Li et al., "Global quantification of mammalian gene expression control," Nature, vol. 473, pp. 337-342, 2011.
  67. A. D. Aragon, G. A. Quiñones, E. V. Thomas, S. Roy, and M. Werner-Washburne, "Release of extraction-resistant mRNA in stationary phase Saccharomyces cerevisiae produces a massive increase in transcript abundance in response to stress," Genome Biology, vol. 7, no. 2, article R9, 2006.
  68. G. Jona, M. Choder, and O. Gileadi, "Glucose starvation induces a drastic reduction in the rates of both transcription and degradation of mRNA in yeast," Biochimica et Biophysica Acta, vol. 1491, no. 1-3, pp. 37-48, 2000.
  69. S. Itzkovitz and and A. van Oudenaarden, "Validating tran- scripts with probes and imaging technology," Nature Methods, vol. 8, pp. S12-S19, 2011.
  70. L. Harel-Sharvit, N. Eldad, G. Haimovich, O. Barkai, L. Duek, and M. Choder, "RNA polymerase II subunits link transcription and mRNA decay to translation," Cell, vol. 143, no. 4, pp. 552-563, 2010.
  71. J. A. Kruk, A. Dutta, and J. Fu, "The multifunctional Ccr4-not complex directly promotes transcription elongation," Genes and Development, vol. 25, no. 6, pp. 581-593, 2011. Submit your manuscripts at http://www.hindawi.com Hindawi Publishing Corporation http://www.hindawi.com Volume 2014