Abstract
Messenger RNA transcription in fungi, particularly in the budding yeast Saccharomyces cerevisiae, is one of the main models for transcriptional research. In this chapter, we review the main mechanisms that operate during fungal RNA polymerase II-dependent transcription, from the initiation step to the termination one. In the elongation phase, processing of the nascent transcript, including 5′ capping, splicing, 3′ end formation and transport, is coupled to transcription. The RNA polymerase II template is not naked DNA, but chromatin. We review the impact of chromatin in the elongation phase and in the phenomenon of RNA polymerase II backtracking. Strikingly, synthesis and degradation have been shown recently to be connected, resulting in a general buffering system for messenger RNA concentration. In this way, messenger RNA synthesis, processing, and degradation are interlinked and have the potential to influence each other.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Adelman K, Marr MT, Werner J, Saunders A, Ni Z, Andrulis ED et al (2005) Efficient release from promoter-proximal stall sites requires transcript cleavage factor TFIIS. Mol Cell 17:103–112
Albert I, Mavrich TN, Tomsho LP, Qi J, Zanton SJ, Schuster SC et al (2007) Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 446:572–576
Arimura Y, Tachiwana H, Oda T, Sato M, Kurumizaka H (2012) Structural analysis of the hexasome, lacking one histone H2A/H2B dimer from the conventional nucleosome. Biochemistry 51:3302–3309
Ast G (2004) How did alternative splicing evolve? Nat Rev Genet 5:773–782
Badarinarayana V, Chiang YC, Denis CL (2000) Functional interaction of CCR4-NOT proteins with TATAA-binding protein (TBP) and its associated factors in yeast. Genetics 155:1045–1054
Bataille AR, Jeronimo C, Jacques PE, Laramee L, Fortin ME, Forest A et al (2012) A universal RNA polymerase II CTD cycle is orchestrated by complex interplays between kinase, phosphatase, and isomerase enzymes along genes. Mol Cell 45:158–170
Bhaumik SR (2011) Distinct regulatory mechanisms of eukaryotic transcriptional activation by SAGA and TFIID. Biochim Biophys Acta 1809:97–108
Bintu L, Kopaczynska M, Hodges C, Lubkowska L, Kashlev M, Bustamante C (2011) The elongation rate of RNA polymerase determines the fate of transcribed nucleosomes. Nat Struct Mol Biol 18:1394–1399
Bloom AL, Solomons JT, Havel VE, Panepinto JC (2013) Uncoupling of mRNA synthesis and degradation impairs adaptation to host temperature in Cryptococcus neoformans. Mol Microbiol 89:65–83
Brahmachari SK, Sarkar PS, Raghavan S, Narayan M, Maiti AK (1997) Polypurine/polypyrimidine sequences as cis-acting transcriptional regulators. Gene 190:17–26
Brannan K, Bentley DL (2012) Control of transcriptional elongation by RNA polymerase II: a retrospective. Genet Res Int 2012:170173
Bregman A, Avraham-Kelbert M, Barkai O, Duek L, Guterman A, Choder M (2011) Promoter elements regulate cytoplasmic mRNA decay. Cell 147:1473–1483
Brill SJ, Sternglanz R (1988) Transcription-dependent DNA supercoiling in yeast DNA topoisomerase mutants. Cell 54:403–411
Cabal GG, Genovesio A, Rodriguez-Navarro S, Zimmer C, Gadal O, Lesne A et al (2006) SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature 441:770–773
Chang HW, Kulaeva OI, Shaytan AK, Kibanov M, Kuznedelov K, Severinov KV et al. (2013) Analysis of the mechanism of nucleosome survival during transcription. Nucleic Acids Res 42(3):1619–1627
Chatterjee N, Sinha D, Lemma-Dechassa M, Tan S, Shogren-Knaak MA, Bartholomew B (2011) Histone H3 tail acetylation modulates ATP-dependent remodeling through multiple mechanisms. Nucleic Acids Res 39:8378–8391
Chavez S, Aguilera A (1997) The yeast HPR1 gene has a functional role in transcriptional elongation that uncovers a novel source of genome instability. Genes Dev 11:3459–3470
Chavez S, Beilharz T, Rondon AG, Erdjument-Bromage H, Tempst P, Svejstrup JQ et al (2000) A protein complex containing Tho2, Hpr1, Mft1 and a novel protein, Thp2, connects transcription elongation with mitotic recombination in Saccharomyces cerevisiae. EMBO J 19:5824–5834
Cheung AC, Cramer P (2011) Structural basis of RNA polymerase II backtracking, arrest and reactivation. Nature 471:249–253
Cheung V, Chua G, Batada NN, Landry CR, Michnick SW, Hughes TR et al (2008) Chromatin- and transcription-related factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biol 6:e277
Choder M (2011) mRNA imprinting: additional level in the regulation of gene expression. Cell Logist 1:37–40
Choder M (2004) Rpb4 and Rpb7: subunits of RNA polymerase II and beyond. Trends Biochem Sci 29:674–681
Churchman LS, Weissman JS (2011) Nascent transcript sequencing visualizes transcription at nucleotide resolution. Nature 469:368–373
Core LJ, Waterfall JJ, Lis JT (2008) Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322:1845–1848
Cramer P (2004) Structure and function of RNA polymerase II. Adv Protein Chem 67:1–42
Dahan N, Choder M (2013) The eukaryotic transcriptional machinery regulates mRNA translation and decay in the cytoplasm. Biochim Biophys Acta 1829:169–173
Dahan O, Gingold H, Pilpel Y (2011) Regulatory mechanisms and networks couple the different phases of gene expression. Trends Genet 27:316–322
Darzacq X, Shav-Tal Y, de Turris V, Brody Y, Shenoy SM, Phair RD et al (2007) In vivo dynamics of RNA polymerase II transcription. Nat Struct Mol Biol 14:796–806
Daulny A, Tansey WP (2009) Damage control: DNA repair, transcription, and the ubiquitin-proteasome system. DNA Repair (Amst) 8:444–448
Deluen C, James N, Maillet L, Molinete M, Theiler G, Lemaire M et al (2002) The Ccr4-not complex and yTAF1 (yTaf(II)130p/yTaf(II)145p) show physical and functional interactions. Mol Cell Biol 22:6735–6749
Denis CL, Chiang YC, Cui Y, Chen J (2001) Genetic evidence supports a role for the yeast CCR4-NOT complex in transcriptional elongation. Genetics 158:627–634
Dori-Bachash M, Shema E, Tirosh I (2011) Coupled evolution of transcription and mRNA degradation. PLoS Biol 9:e1001106
Engel C, Sainsbury S, Cheung AC, Kostrewa D, Cramer P (2013) RNA polymerase I structure and transcription regulation. Nature 502:650–655
Farago M, Nahari T, Hammel C, Cole CN, Choder M (2003) Rpb4p, a subunit of RNA polymerase II, mediates mRNA export during stress. Mol Biol Cell 14:2744–2755
Fazzio TG, Kooperberg C, Goldmark JP, Neal C, Basom R, Delrow J et al (2001) Widespread collaboration of Isw2 and Sin3-Rpd3 chromatin remodeling complexes in transcriptional repression. Mol Cell Biol 21:6450–6460
Fernandez-Tornero C, Moreno-Morcillo M, Rashid UJ, Taylor NM, Ruiz FM, Gruene T et al (2013) Crystal structure of the 14-subunit RNA polymerase I. Nature 502:644–649
Fish RN, Kane CM (2002) Promoting elongation with transcript cleavage stimulatory factors. Biochim Biophys Acta 1577:287–307
Gaillard H, Tous C, Botet J, Gonzalez-Aguilera C, Quintero MJ, Viladevall L et al (2009) Genome-wide analysis of factors affecting transcription elongation and DNA repair: a new role for PAF and Ccr4-not in transcription-coupled repair. PLoS Genet 5:e1000364
Gilchrist DA, Fargo DC, Adelman K (2009) Using ChIP-chip and ChIP-seq to study the regulation of gene expression: genome-wide localization studies reveal widespread regulation of transcription elongation. Methods 48:398–408
Goler-Baron V, Selitrennik M, Barkai O, Haimovich G, Lotan R, Choder M (2008) Transcription in the nucleus and mRNA decay in the cytoplasm are coupled processes. Genes Dev 22:2022–2027
Gomez-Herreros F, de Miguel-Jimenez L, Millan-Zambrano G, Penate X, Delgado-Ramos L, Munoz-Centeno MC et al (2012a) One step back before moving forward: regulation of transcription elongation by arrest and backtracking. FEBS Lett 586:2820–2825
Gomez-Herreros F, de Miguel-Jimenez L, Morillo-Huesca M, Delgado-Ramos L, Munoz-Centeno MC, and Chavez S (2012b) TFIIS is required for the balanced expression of the genes encoding ribosomal components under transcriptional stress. Nucleic Acids Res 40(14):6508–6519
Grant PA, Duggan L, Cote J, Roberts SM, Brownell JE, Candau R et al (1997) Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev 11:1640–1650
Grunberg S, Hahn S (2013) Structural insights into transcription initiation by RNA polymerase II. Trends Biochem Sci 38:603–611
Gu W, Reines D (1995) Identification of a decay in transcription potential that results in elongation factor dependence of RNA polymerase II. J Biol Chem 270:11238–11244
Guarente L (1988) UASs and enhancers: common mechanism of transcriptional activation in yeast and mammals. Cell 52:303–305
Haimovich G, Medina DA, Causse SZ, Garber M, Millan-Zambrano G, Barkai O et al (2013) Gene expression is circular: factors for mRNA degradation also foster mRNA synthesis. Cell 153:1000–1011
Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, Danford TW et al (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431:99–104
Harel-Sharvit L, Eldad N, Haimovich G, Barkai O, Duek L, Choder M (2010) RNA polymerase II subunits link transcription and mRNA decay to translation. Cell 143:552–563
Hsin JP, Manley JL (2012) The RNA polymerase II CTD coordinates transcription and RNA processing. Genes Dev 26:2119–2137
Huertas P, Aguilera A (2003) Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol Cell 12:711–721
Izban MG, Luse DS (1992) The RNA polymerase II ternary complex cleaves the nascent transcript in a 3’–5’ direction in the presence of elongation factor SII. Genes Dev 6:1342–1356
Izban MG, Luse DS (1991) Transcription on nucleosomal templates by RNA polymerase II in vitro: inhibition of elongation with enhancement of sequence-specific pausing. Genes Dev 5:683–696
Jeronimo C, Bataille AR, Robert F (2013) The writers, readers, and functions of the RNA polymerase II C-Terminal Domain Code. Chem Rev 113(11):8491–8522
Johnson SA, Kim H, Erickson B, Bentley DL (2011) The export factor Yra1 modulates mRNA 3’ end processing. Nat Struct Mol Biol 18:1164–1171
Joshi RS, Pina B, Roca J (2012) Topoisomerase II is required for the production of long Pol II gene transcripts in yeast. Nucleic Acids Res 40:7907–7915
Kim H, Erickson B, Luo W, Seward D, Graber JH, Pollock DD et al (2010) Gene-specific RNA polymerase II phosphorylation and the CTD code. Nat Struct Mol Biol 17:1279–1286
Kireeva ML, Hancock B, Cremona GH, Walter W, Studitsky VM, Kashlev M (2005) Nature of the nucleosomal barrier to RNA polymerase II. Mol Cell 18:97–108
Klages N, Strubin M (1995) Stimulation of RNA polymerase II transcription initiation by recruitment of TBP in vivo. Nature 374:822–823
Komili S, Silver PA (2008) Coupling and coordination in gene expression processes: a systems biology view. Nat Rev Genet 9:38–48
Kornberg RD (2007) The molecular basis of eukaryotic transcription. Proc Natl Acad Sci USA 104:12955–12961
Kruk JA, Dutta A, Fu J, Gilmour DS, Reese JC (2011) The multifunctional Ccr4-Not complex directly promotes transcription elongation. Genes Dev 25:581–593
Kubicek K, Cerna H, Holub P, Pasulka J, Hrossova D, Loehr F et al (2012) Serine phosphorylation and proline isomerization in RNAP II CTD control recruitment of Nrd1. Genes Dev 26:1891–1896
Kulaeva OI, Gaykalova DA, Pestov NA, Golovastov VV, Vassylyev DG, Artsimovitch I et al (2009) Mechanism of chromatin remodeling and recovery during passage of RNA polymerase II. Nat Struct Mol Biol 16:1272–1278
Kupfer DM, Drabenstot SD, Buchanan KL, Lai H, Zhu H, Dyer DW et al (2004) Introns and splicing elements of five diverse fungi. Eukaryot Cell 3:1088–1100
Kuryan BG, Kim J, Tran NN, Lombardo SR, Venkatesh S, Workman JL et al (2012) Histone density is maintained during transcription mediated by the chromatin remodeler RSC and histone chaperone NAP1 in vitro. Proc Natl Acad Sci USA 109:1931–1936
Liu P, Kenney JM, Stiller JW, Greenleaf AL (2010) Genetic organization, length conservation, and evolution of RNA polymerase II carboxyl-terminal domain. Mol Biol Evol 27:2628–2641
Lorch Y, Maier-Davis B, Kornberg RD (2006) Chromatin remodeling by nucleosome disassembly in vitro. Proc Natl Acad Sci USA 103:3090–3093
Lotan R, Bar-On VG, Harel-Sharvit L, Duek L, Melamed D, Choder M (2005) The RNA polymerase II subunit Rpb4p mediates decay of a specific class of mRNAs. Genes Dev 19:3004–3016
Lotan R, Goler-Baron V, Duek L, Haimovich G, Choder M (2007) The Rpb7p subunit of yeast RNA polymerase II plays roles in the two major cytoplasmic mRNA decay mechanisms. J Cell Biol 178:1133–1143
Luse DS, Spangler LC, Ujvari A (2011) Efficient and rapid nucleosome traversal by RNA polymerase II depends on a combination of transcript elongation factors. J Biol Chem 286:6040–6048
Margaritis T, Holstege FC (2008) Poised RNA polymerase II gives pause for thought. Cell 133:581–584
Mason PB, Struhl K (2005) Distinction and relationship between elongation rate and processivity of RNA polymerase II in vivo. Mol Cell 17:831–840
Mayer A, Heidemann M, Lidschreiber M, Schreieck A, Sun M, Hintermair C et al (2012) CTD tyrosine phosphorylation impairs termination factor recruitment to RNA polymerase II. Science 336:1723–1725
Millan-Zambrano G, Rodriguez-Gil A, Penate X, de Miguel-Jimenez L, Morillo-Huesca M, Krogan N et al (2013) The prefoldin complex regulates chromatin dynamics during transcription elongation. PLoS Genet 9:e1003776
Mitra D, Parnell EJ, Landon JW, Yu Y, Stillman DJ (2006) SWI/SNF binding to the HO promoter requires histone acetylation and stimulates TATA-binding protein recruitment. Mol Cell Biol 26:4095–4110
Morris DP, Greenleaf AL (2000) The splicing factor, Prp40, binds the phosphorylated carboxyl-terminal domain of RNA polymerase II. J Biol Chem 275:39935–39943
Papai G, Weil PA, Schultz P (2011) New insights into the function of transcription factor TFIID from recent structural studies. Curr Opin Genet Dev 21:219–224
Parker R, Sheth U (2007) P bodies and the control of mRNA translation and degradation. Mol Cell 25:635–646
Pelechano V, Jimeno-Gonzalez S, Rodriguez-Gil A, Garcia-Martinez J, Perez-Ortin JE, Chavez S (2009) Regulon-specific control of transcription elongation across the yeast genome. PLoS Genet 5:e1000614
Pelechano V, Wei W, Steinmetz LM (2013) Extensive transcriptional heterogeneity revealed by isoform profiling. Nature 497:127–131
Perales R, Bentley D (2009) “Cotranscriptionality”: the transcription elongation complex as a nexus for nuclear transactions. Mol Cell 36:178–191
Perez-Ortin JE, Alepuz P, Chavez S, Choder M (2013) Eukaryotic mRNA decay: methodologies, pathways, and links to other stages of gene expression. J Mol Biol 425:3750–3775
Perez-Ortin JE, de Miguel-Jimenez L, Chavez S (2011) Genome-wide studies of mRNA synthesis and degradation in eukaryotes. Biochim Biophys Acta 1819:604
Phatnani HP, Jones JC, Greenleaf AL (2004) Expanding the functional repertoire of CTD kinase I and RNA polymerase II: novel phosphoCTD-associating proteins in the yeast proteome. Biochemistry 43:15702–15719
Powell W, Reines D (1996) Mutations in the second largest subunit of RNA polymerase II cause 6-azauracil sensitivity in yeast and increased transcriptional arrest in vitro. J Biol Chem 271:6866–6873
Pugh BF (2000) Control of gene expression through regulation of the TATA-binding protein. Gene 255:1–14
Rhee HS, Pugh BF (2012) Genome-wide structure and organization of eukaryotic pre-initiation complexes. Nature 483:295–301
Richard P, Manley JL (2009) Transcription termination by nuclear RNA polymerases. Genes Dev 23:1247–1269
Rodriguez CR, Cho EJ, Keogh MC, Moore CL, Greenleaf AL, Buratowski S (2000) Kin28, the TFIIH-associated carboxy-terminal domain kinase, facilitates the recruitment of mRNA processing machinery to RNA polymerase II. Mol Cell Biol 20:104–112
Rodriguez-Gil A, Garcia-Martinez J, Pelechano V, Munoz-Centeno Mde L, Geli V, Perez-Ortin JE et al (2010) The distribution of active RNA polymerase II along the transcribed region is gene-specific and controlled by elongation factors. Nucleic Acids Res 38:4651–4664
Rodriguez-Navarro S (2009) Insights into SAGA function during gene expression. EMBO Rep 10:843–850
Schwabish MA, Struhl K (2006) Asf1 mediates histone eviction and deposition during elongation by RNA polymerase II. Mol Cell 22:415–422
Schwabish MA, Struhl K (2004) Evidence for eviction and rapid deposition of histones upon transcriptional elongation by RNA polymerase II. Mol Cell Biol 24:10111–10117
Selitrennik M, Duek L, Lotan R, Choder M (2006) Nucleocytoplasmic shuttling of the Rpb4p and Rpb7p subunits of Saccharomyces cerevisiae RNA polymerase II by two pathways. Eukaryot Cell 5:2092–2103
Sigurdsson S, Dirac-Svejstrup AB, Svejstrup JQ (2010) Evidence that transcript cleavage is essential for RNA polymerase II transcription and cell viability. Mol Cell 38:202–210
Singh BN, Hampsey M (2007) A transcription-independent role for TFIIB in gene looping. Mol Cell 27:806–816
Sogaard TM, Svejstrup JQ (2007) Hyperphosphorylation of the C-terminal repeat domain of RNA polymerase II facilitates dissociation of its complex with mediator. J Biol Chem 282:14113–14120
Somesh BP, Reid J, Liu WF, Sogaard TM, Erdjument-Bromage H, Tempst P et al (2005) Multiple mechanisms confining RNA polymerase II ubiquitylation to polymerases undergoing transcriptional arrest. Cell 121:913–923
Steinmetz EJ, Brow DA (1998) Control of pre-mRNA accumulation by the essential yeast protein Nrd1 requires high-affinity transcript binding and a domain implicated in RNA polymerase II association. Proc Natl Acad Sci USA 95:6699–6704
Stewart M (2010) Nuclear export of mRNA. Trends Biochem Sci 35:609–617
Struhl K, Segal E (2013) Determinants of nucleosome positioning. Nat Struct Mol Biol 20:267–273
Sun M, Schwalb B, Pirkl N, Maier KC, Schenk A, Failmezger H et al (2013) Global analysis of eukaryotic mRNA degradation reveals Xrn1-dependent buffering of transcript levels. Mol Cell 52:52–62
Sun M, Schwalb B, Schulz D, Pirkl N, Etzold S, Lariviere L et al (2012) Comparative dynamic transcriptome analysis (cDTA) reveals mutual feedback between mRNA synthesis and degradation. Genome Res 22:1350–1359
Takahata S, Yu Y, Stillman DJ (2009) The E2F functional analogue SBF recruits the Rpd3(L) HDAC, via Whi5 and Stb1, and the FACT chromatin reorganizer, to yeast G1 cyclin promoters. EMBO J 28:3378–3389
Thomas MC, Chiang CM (2006) The general transcription machinery and general cofactors. Crit Rev Biochem Mol Biol 41:105–178
Tjian R (1978) The binding site on SV40 DNA for a T antigen-related protein. Cell 13:165–179
Trcek T, Larson DR, Moldon A, Query CC, Singer RH (2011) Single-molecule mRNA decay measurements reveal promoter- regulated mRNA stability in yeast. Cell 147:1484–1497
Tsankov A, Yanagisawa Y, Rhind N, Regev A, Rando OJ (2011) Evolutionary divergence of intrinsic and trans-regulated nucleosome positioning sequences reveals plastic rules for chromatin organization. Genome Res 21:1851–1862
Tucker M, Staples RR, Valencia-Sanchez MA, Muhlrad D, Parker R (2002) Ccr4p is the catalytic subunit of a Ccr4p/Pop2p/Notp mRNA deadenylase complex in Saccharomyces cerevisiae. EMBO J 21:1427–1436
Vannini A, Cramer P (2012) Conservation between the RNA polymerase I, II, and III transcription initiation machineries. Mol Cell 45:439–446
Vasiljeva L, Kim M, Mutschler H, Buratowski S, Meinhart A (2008) The Nrd1-Nab3-Sen1 termination complex interacts with the Ser5-phosphorylated RNA polymerase II C-terminal domain. Nat Struct Mol Biol 15:795–804
Venters BJ, Pugh BF (2009a) A canonical promoter organization of the transcription machinery and its regulators in the Saccharomyces genome. Genome Res 19:360–371
Venters BJ, Pugh BF (2009b) How eukaryotic genes are transcribed. Crit Rev Biochem Mol Biol 44:117–141
Weiner A, Hughes A, Yassour M, Rando OJ, Friedman N (2010) High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res 20:90–100
Yuan GC, Liu YJ, Dion MF, Slack MD, Wu LF, Altschuler SJ et al (2005) Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309:626–630
Zhang DW, Mosley AL, Ramisetty SR, Rodriguez-Molina JB, Washburn MP, Ansari AZ (2012) Ssu72 phosphatase-dependent erasure of phospho-Ser7 marks on the RNA polymerase II C-terminal domain is essential for viability and transcription termination. J Biol Chem 287:8541–8551
Zhang Z, Pugh BF (2011) High-resolution genome-wide mapping of the primary structure of chromatin. Cell 144:175–186
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Peñate, X., Chávez, S. (2014). RNA Polymerase II-Dependent Transcription in Fungi and Its Interplay with mRNA Decay. In: Sesma, A., von der Haar, T. (eds) Fungal RNA Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-05687-6_1
Download citation
DOI: https://doi.org/10.1007/978-3-319-05687-6_1
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-05686-9
Online ISBN: 978-3-319-05687-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)