Emerging roles for RNA polymerase II CTD in Arabidopsis

Trends in Plant Science

Volumn 18, Issue 11, 2013, Pages 633-643

  Hajheidari, Mohsen ^a   Koncz, Csaba ^a,b   Eick, Dirk ^c  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b INSTITUTE OF BIOCHEMISTRY   (Hungary)

^c Munich Center for Integrated Protein Science   (Germany)

Author keywords

CTD kinase; Histone mark; MiRNA; RNA polymerase II CTD; RNA processing; Transcription

Indexed keywords

ARABIDOPSIS; MAMMALIA;

ARABIDOPSIS PROTEIN; CARBOXY TERMINAL DOMAIN KINASE; CARBOXY TERMINAL DOMAIN PHOSPHATASE; CARBOXY-TERMINAL DOMAIN KINASE; CARBOXY-TERMINAL DOMAIN PHOSPHATASE; MICRORNA; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE; RNA POLYMERASE II;

ANIMAL; ARABIDOPSIS; BIOLOGICAL MODEL; CTD KINASE; ENZYMOLOGY; GENETIC TRANSCRIPTION; GENETICS; HISTONE MARK; HUMAN; MAMMAL; METABOLISM; PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN TERTIARY STRUCTURE; REVIEW; RNA POLYMERASE II CTD; RNA PROCESSING; SACCHAROMYCES CEREVISIAE; SPECIES DIFFERENCE; TRANSCRIPTION;

CTD KINASE; HISTONE MARK; MIRNA; RNA POLYMERASE II CTD; RNA PROCESSING; TRANSCRIPTION;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; HUMANS; MAMMALS; MODELS, BIOLOGICAL; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SPECIES SPECIFICITY; TRANSCRIPTION, GENETIC;

EID: 84887017354     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2013.07.001     Document Type: Review

References (122)

1. Allison L.A., et al. The C-terminal domain of the largest subunit of RNA polymerase II of Saccharomyces cerevisiae, Drosophila melanogaster, and mammals: a conserved structure with an essential function. Mol. Cell. Biol. 1988, 8:321-329.
2. Nawrath C., et al. Homologous domains of the largest subunit of eucaryotic RNA polymerase II are conserved in plants. Mol. Gen. Genet. 1990, 223:65-75.
3. Luo J., Hall B.D. A multistep process gave rise to RNA polymerase IV of land plants. J. Mol. Evol. 2007, 64:101-112.
4. Ream T.S., et al. Subunit compositions of the RNA-silencing enzymes Pol IV and Pol V reveal their origins as specialized forms of RNA polymerase II. Mol. Cell 2009, 33:192-203.
5. Haag J.R., et al. In vitro transcription activities of Pol IV, Pol V, and RDR2 reveal coupling of Pol IV and RDR2 for dsRNA synthesis in plant RNA silencing. Mol. Cell 2012, 48:811-818.
6. Haag J.R., Pikaard C.S. Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat. Rev. Mol. Cell Biol. 2011, 12:483-492.
7. Chapman R.D., et al. The last CTD repeat of the mammalian RNA polymerase II large subunit is important for its stability. Nucleic Acids Res. 2004, 32:35-44.
8. Koiwa H., et al. Arabidopsis C-terminal domain phosphatase-like 1 and 2 are essential Ser-5-specific C-terminal domain phosphatases. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:14539-14544.
9. Stiller J.W., Cook M.S. Functional unit of the RNA polymerase II C-terminal domain lies within heptapeptide pairs. Eukaryot. Cell 2004, 3:735-740.
10. Meinhart A., et al. A structural perspective of CTD function. Genes Dev. 2005, 19:1401-14156.
11. Buratowski S. Progression through the RNA polymerase II CTD cycle. Mol. Cell 2009, 36:541-546.
12. Egloff S., et al. Updating the RNA polymerase CTD code: adding gene-specific layers. Trends Genet. 2012, 28:333-341.
13. Hsin J.P., Manley J.L. The RNA polymerase II CTD coordinates transcription and RNA processing. Genes Dev. 2012, 26:2119-2137.
14. Akhtar M.S., et al. TFIIH kinase places bivalent marks on the carboxy-terminal domain of RNA polymerase II. Mol. Cell 2009, 34:387-393.
15. Egloff S., et al. The integrator complex recognizes a new double mark on the RNA polymerase II carboxyl-terminal domain. J. Biol. Chem. 2010, 285:20564-20569.
16. Hampsey M., Reinberg D. Tails of intrigue: phosphorylation of RNA polymerase II mediates histone methylation. Cell 2003, 113:429-432.
17. Max T., et al. Hyperphosphorylation of the carboxyterminal repeat domain of RNA polymerase II facilitates dissociation of its complex with mediator. J. Biol. Chem. 2007, 282:14113-14120.
18. Boeing S., et al. RNA polymerase II C-terminal heptarepeat domain Ser-7 phosphorylation is established in a mediator-dependent fashion. J. Biol. Chem. 2010, 285:188-196.
19. Perales R., Bentley D. "Cotranscriptionality": the transcription elongation complex as a nexus for nuclear transactions. Mol. Cell 2009, 36:178-191.
20. Wood A., et al. The Paf1 complex is essential for histone monoubiquitination by the Rad6-Bre1 complex, which signals for histone methylation by COMPASS and Dot1p. J. Biol. Chem. 2003, 278:34739-34742.
21. Wood A., et al. The Bur1/Bur2 complex is required for histone H2B monoubiquitination by Rad6/Bre1 and histone methylation by COMPASS. Mol. Cell 2005, 20:589-599.
22. Qiu H., et al. The Spt4p subunit of yeast DSIF stimulates association of the Paf1 complex with elongating RNA polymerase II. Mol. Cell. Biol. 2006, 26:3135-3148.
23. Qiu H., et al. Phosphorylation of the Pol II CTD by KIN28 enhances BUR1/BUR2 recruitment and Ser2 CTD phosphorylation near promoters. Mol. Cell 2009, 33:752-762.
24. Ng H.H., et al. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell 2003, 11:709-719.
25. Laribee R.N., et al. BUR kinase selectively regulates H3 K4 trimethylation and H2B ubiquitylation through recruitment of the PAF elongation complex. Curr. Biol. 2005, 15:1487-1493.
26. Li B., et al. The role of chromatin during transcription. Cell 2007, 128:707-719.
27. Kim T., Buratowski S. Dimethylation of H3K4 by Set1 recruits the Set3 histone deacetylase complex to 5' transcribed regions. Cell 2009, 137:259-272.
28. Eissenberg J.C., Shilatifard A. Histone H3 lysine 4 (H3K4) methylation in development and differentiation. Dev. Biol. 2010, 339:240-249.
29. Shilatifard A. The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu. Rev. Biochem. 2012, 81:65-95.
30. Carrozza M.J., et al. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 2005, 123:581-592.
31. Keogh M.C., et al. Cotranscriptional Set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 2005, 123:593-605.
32. Pray-Grant M.G., et al. Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. Nature 2005, 433:434-438.
33. Govind C.K., et al. Gcn5 promotes acetylation, eviction, and methylation of nucleosomes in transcribed coding regions. Mol. Cell 2007, 25:31-42.
34. Govind C.K., et al. Phosphorylated Pol II CTD recruits multiple HDACs, including Rpd3C(S), for methylation-dependent deacetylation of ORF nucleosomes. Mol. Cell 2010, 39:234-246.
35. Komarnitsky P., et al. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev. 2000, 14:2452-2460.
36. Schwer B., Shuman S. Deciphering the RNA polymerase II CTD code in fission yeast. Mol. Cell 2011, 43:311-318.
37. Gu M., et al. Structure of the Saccharomyces cerevisiae Cet1-Ceg1 mRNA capping apparatus. Structure 2010, 18:216-227.
38. Shimotohno A., et al. The plant-specific kinase CDKF;1 is involved in activating phosphorylation of cyclin-dependent kinase-activating kinases in Arabidopsis. Plant Cell 2004, 16:2954-2966.
39. Shimotohno A., et al. Diverse phosphoregulatory mechanisms controlling cyclin-dependent kinase-activating kinases in Arabidopsis. Plant J. 2006, 47:701-710.
40. Van Leene J., et al. Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol. Syst. Biol. 2010, 6:397-408.
41. Hajheidari M., et al. CDKF;1 and CDKD protein kinases regulate phosphorylation of serine residues in the C-terminal domain of Arabidopsis RNA polymerase II. Plant Cell 2012, 24:1626-1642.
42. Laubinger S., et al. Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:8795-8800.
43. Nielsen A.F., et al. Ars2 and the cap-binding complex team up for silencing. Cell 2009, 138:224-226.
44. Wang L., et al. NOT2 proteins promote polymerase II-dependent transcription and interact with multiple microRNA biogenesis factors in Arabidopsis. Plant Cell 2013, 10.1105/tpc.112.105882.
45. Park S., et al. PLANT HOMOLOGOUS TO PARAFIBROMIN is a component of the Paf1 complex and assists in regulating expression of genes within H3K27me3-enriched chromatin. Plant Physiol. 2010, 153:821-831.
46. Yu X., Michaels S.D. The Arabidopsis Paf1c complex component CDC73 participates in the modification of FLOWERING LOCUS C chromatin. Plant Physiol. 2010, 153:1074-1084.
47. Ng H.H., et al. The Rtf1 component of the Paf1 transcriptional elongation complex is required for ubiquitination of histone H2B. J. Biol. Chem. 2003, 278:33625-33628.
48. Cao Y., Ma L. Conservation and divergence of the histone H2B monoubiquitination pathway from yeast to humans and plants. Front. Biol. 2011, 6:109-117.
49. Cao Y., et al. Histone H2B Monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell 2008, 20:2586-2602.
50. Lolas I.B., et al. The transcript elongation factor FACT affects Arabidopsis vegetative and reproductive development and functionally interacts with HUB1/2. Plant J. 2010, 61:686-697.
51. Veerappan C.S., et al. Evolution of SET-domain protein families in the unicellular and multicellular Ascomycota fungi. BMC Evol. Biol. 2008, 8:190-210.
52. Ding Y., et al. Two distinct roles of ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1) at promoters and within transcribed regions of ATX1-regulated genes. Plant Cell 2011, 23:350-363.
53. Feng S., Jacobsen S.E. Epigenetic modifications in plants: an evolutionary perspective. Curr. Opin. Plant Biol. 2011, 14:179-186.
54. Bartkowiak B., et al. CDK12 is a transcription elongation-associated CTD kinase, the metazoan ortholog of yeast Ctk1. Genes Dev. 2010, 24:2303-2316.
55. Devaiah B.N., et al. BRD4 is an atypical kinase that phosphorylates serine-2 of the RNA polymerase II carboxy-terminal domain. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:6927-6932.
56. Core L.J., Lis J.T. Transcription regulation through promoter-proximal pausing of RNA polymerase II. Science 2008, 319:1791-1792.
57. Levine M. Paused RNA polymerase II as a developmental checkpoint. Cell 2011, 145:502-511.
58. Takahashi H., et al. Human Mediator subunit MED26 functions as a docking site for transcription elongation factors. Cell 2011, 146:92-104.
59. Schwartz J.C., et al. FUS binds the CTD of RNA polymerase II and regulates its phosphorylation at Ser2. Genes Dev. 2012, 26:2690-2695.
60. Byers S.A., et al. HEXIM2, a HEXIM1-related protein, regulates positive transcription elongation factor b through association with 7SK. J. Biol. Chem. 2005, 280:16360-16367.
61. Lenasi T., Barboric M. P-TEFb stimulates transcription elongation and pre-mRNA splicing through multilateral mechanisms. RNA Biol. 2010, 7:145-150.
62. Wyce A., et al. H2B ubiquitylation acts as a barrier to Ctk1 nucleosomal recruitment prior to removal by Ubp8 within a SAGA-related complex. Mol. Cell 2007, 27:275-288.
63. Wood A., et al. Ctk complex-mediated regulation of histone methylation by COMPASS. Mol. Cell. Biol. 2007, 27:709-720.
64. Yoh S.M., et al. The Spt6 SH2 domain binds Ser2-P RNAPII to direct Iws1-dependent mRNA splicing and export. Genes Dev. 2007, 21:160-174.
65. Yoh S.M., et al. The Iws1:Spt6:CTD complex controls cotranscriptional mRNA biosynthesis and HYPB/Setd2-mediated histone H3K36 methylation. Genes Dev. 2008, 22:3422-3434.
66. Zhang L., et al. Spn1 regulates the recruitment of Spt6 and the Swi/Snf complex during transcriptional activation by RNA polymerase II. Mol. Cell. Biol. 2008, 28:1393-1403.
67. Sun M., et al. A tandem SH2 domain in transcription elongation factor Spt6 binds the phosphorylated RNA polymerase II C-terminal repeat domain (CTD). J. Biol. Chem. 2010, 285:41597-41603.
68. Mayer A., et al. CTD tyrosine phosphorylation impairs termination factor recruitment to RNA polymerase II. Science 2012, 336:1723-1725.
69. MacKellar A.L., Greenleaf A.L. Cotranscriptional association of mRNA export factor Yra1 with C-terminal domain of RNA polymerase II. J. Biol. Chem. 2011, 286:36385-36395.
70. Hirose Y., Manley J.L. RNA polymerase II and the integration of nuclear events. Genes Dev. 2000, 14:1415-1429.
71. Gasch A., et al. The structure of Prp40 FF1 domain and its interaction with the crn-TPR1 motif of Clf1 gives a new insight into the binding mode of FF domains. J. Biol. Chem. 2006, 281:356-364.
72. David C.J., et al. The RNA polymerase II C-terminal domain promotes splicing activation through recruitment of a U2AF65-Prp19 complex. Genes Dev. 2011, 25:972-983.
73. Rosonina E., et al. Role for PSF in mediating transcriptional activator-dependent stimulation of pre-mRNA processing in vivo. Mol. Cell. Biol. 2005, 25:6734-6746.
74. Sanchez-Alvarez M., et al. Human transcription elongation factor CA150 localizes to splicing factor-rich nuclear speckles and assembles transcription and splicing components into complexes through its amino and carboxyl regions. Mol. Cell. Biol. 2006, 26:4998-5014.
75. Cui X., et al. Roles of Arabidopsis cyclin-dependent kinase C complexes in cauliflower mosaic virus infection, plant growth, and development. Plant Cell 2007, 19:1388-1402.
76. He X.J., et al. An effector of RNA-directed DNA methylation in Arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell 2009, 137:498-508.
77. Bies-Etheve N., et al. RNA-directed DNA methylation requires an AGO4-interacting member of the SPT5 elongation factor family. EMBO Rep. 2009, 10:649-654.
78. Rowley M.J., et al. Independent chromatin binding of ARGONAUTE4 and SPT5L/KTF1 mediates transcriptional gene silencing. PLoS Genet. 2011, 7:e1002120.
79. Kiely C.M., et al. Spt6 of S. pombe is required for heterochromatic silencing. Mol. Cell. Biol. 2011, 31:4193-4204.
80. Gu X., et al. SPT6L encoding a putative WG/GW-repeat protein regulates apical-basal polarity of embryo in Arabidopsis. Mol. Plant 2012, 5:249-259.
81. Li L., et al. Arabidopsis IWS1 interacts with transcription factor BES1 and is involved in plant steroid hormone brassinosteroid regulated gene expression. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:3918-3923.
82. Wang B.B., Brendel V. The ASRG database: identification and survey of Arabidopsis thaliana genes involved in pre-mRNA splicing. Genome Biol. 2004, 5:102.1-102.23.
83. Kang C.H., et al. Arabidopsis thaliana PRP40s are RNA polymerase II C-terminal domain-associating proteins. Arch. Biochem. Biophys. 2009, 484:30-38.
84. McCracken S., et al. The C-terminal domain of RNA polymerase II couples messenger RNA processing to transcription. Nature 1997, 385:357-361.
85. Lunde B.M., et al. Cooperative interaction of transcription termination factors with the RNA polymerase II C-terminal domain. Nat. Struct. Mol. Biol. 2010, 17:1195-1201.
86. Dichtl B., et al. Yhh1p/Cft1p directly links poly(A) site recognition and RNA polymerase II transcription termination. EMBO J. 2002, 21:4125-4135.
87. Vasiljeva L., et al. The Nrd1-Nab3-Sen1 termination complex interacts with the Ser5-phosphorylated RNA polymerase II C-terminal domain. Nat. Struct. Mol. Biol. 2008, 15:795-804.
88. Kubicek K., et al. Serine phosphorylation and proline isomerization in RNAP II CTD control recruitment of Nrd1. Genes Dev. 2012, 26:1891-1896.
89. Quesada V., et al. Autoregulation of the site of 3' end formation in FCA pre-mRNA prevents precocious flowering. EMBO J. 2003, 22:3142-3152.
90. Hornyik C., et al. The spen family protein FPA controls alternative cleavage and polyadenylation of RNA. Dev. Cell 2010, 18:203-213.
91. Liu F., et al. Targeted 3' processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 2010, 327:94-97.
92. Sonmez C., et al. RNA 3' processing functions of Arabidopsis FCA and FPA limit intergenic transcription. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:8508-8513.
93. Xing D., et al. Arabidopsis PCFS4, a homolog of yeast polyadenylation factor Pcf11p, regulates FCA alternative processing and promotes flowering time. Plant J. 2008, 54:899-910.
94. Egloff S., et al. Ser7 phosphorylation of the CTD recruits the RPAP2 Ser5 phosphatase to snRNA genes. Mol. Cell 2012, 45:111-122.
95. Kerk D., et al. Evolutionary radiation pattern of novel protein phosphatases revealed by analysis of protein data from the completely sequenced genomes of humans, green algae, and higher plants. Plant Physiol. 2008, 146:351-367.
96. Moorhead G.B., et al. Evolution of protein phosphatases in plants and animals. Biochem. J. 2009, 417:401-409.
97. Kamenski T., et al. Structure and mechanism of RNA polymerase II CTD phosphatases. Mol. Cell 2004, 15:399-407.
98. Ghosh A., et al. The structure of Fcp1, an essential RNA polymerase II CTD phosphatase. Mol. Cell 2008, 32:478-490.
99. Yeo M., et al. Small CTD phosphatases function in silencing neuronal gene expression. Science 2005, 307:596-600.
100. Krishnamurthy S., et al. Ssu72 is an RNA polymerase II CTD phosphatase. Mol. Cell 2004, 14:387-394.
101. Werner-Allen J.W., et al. Cis-proline-mediated Ser(P)5 dephosphorylation by the RNA polymerase II C-terminal domain phosphatase Ssu72. J. Biol. Chem. 2011, 286:5717-5726.
102. Bataille A.R., et al. A universal RNA polymerase II CTD cycle is orchestrated by complex interplays between kinase, phosphatase, and isomerase enzymes along genes. Mol. Cell 2012, 45:158-170.
103. Zhang D.W., et al. Emerging views on the CTD code. Genet. Res. Int. 2012, 2012:347214.
104. Mosley A.L., et al. Rtr1 is a CTD phosphatase that regulates RNA polymerase II during the transition from serine 5 to serine 2 phosphorylation. Mol. Cell 2009, 34:168-178.
105. Xiang K., et al. The yeast regulator of transcription protein Rtr1 lacks an active site and phosphatase activity. Nat. Commun. 2012, 3:946.
106. Aksoy E., et al. Loss of function of Arabidopsis C-terminal domain phosphatase-like1 activates iron deficiency responses at the transcriptional level. Plant Physiol. 2013, 161:330-345.
107. Koiwa H., et al. C-terminal domain phosphatase-like family members (AtCPLs) differentially regulate Arabidopsis thaliana abiotic stress signaling, growth and development. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:10893-10898.
108. Ueda A., et al. The Arabidopsis thaliana carboxyl-terminal domain phosphatase-like 2 regulates plant growth, stress and auxin responses. Plant Mol. Biol. 2008, 67:683-697.
109. Matsuda O., et al. CTD phosphatases in the attenuation of wound-induced transcription of jasmonic acid biosynthetic genes in Arabidopsis. Plant J. 2009, 57:96-108.
110. Bang W., et al. Arabidopsis carboxyl-terminal domain phosphatase-like isoforms share common catalytic and interaction domains but have distinct in planta functions. Plant Physiol. 2006, 142:586-594.
111. Feng Y., et al. Arabidopsis SCP1-like small phosphatases differentially dephosphorylate RNA polymerase II C-terminal domain. Biochem. Biophys. Res. Commun. 2010, 397:355-360.
112. Jin Y-M., et al. AtCPL5, a novel Ser-2-specific RNA polymerase II C-terminal domain phosphatase, positively regulates ABA and drought responses in Arabidopsis. New Phytol. 2011, 190:57-74.
113. Manavella P.A., et al. Fast-forward genetics identifies plant CPL phosphatases as regulators of miRNA processing factor HYL1. Cell 2012, 151:859-870.
114. Venters B.J., Pugh B.F. How eukaryotic genes are transcribed. Crit. Rev. Biochem. Mol. Biol. 2009, 44:117-141.
115. Bartkowiak B., Greenleaf A.L. Phosphorylation of RNAPII: To P-TEFb or not to P-TEFb?. Transcription 2011, 2:115-119.
116. Drogat J., Hermand D. Gene-specific requirement of RNA polymerase II CTD phosphorylation. Mol. Microbiol. 2012, 84:995-1004.
117. Clemente-Blanco A., et al. Cdc14 phosphatase promotes segregation of telomeres through repression of RNA polymerase II transcription. Nat. Cell Biol. 2011, 13:1450-1456.
118. Hintermair C., et al. Threonine-4 of mammalian RNA polymerase II CTD is targeted by Polo-like kinase 3 and required for transcriptional elongation. EMBO J. 2012, 31:2784-2797.
119. Hsin J.P., et al. RNAP II CTD phosphorylated on threonine-4 is required for histone mRNA 3' end processing. Science 2011, 334:683-686.
120. Chapman R.D., et al. Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science 2007, 318:1780-1782.
121. Stiller J.W., et al. Evolutionary complementation for polymerase II CTD function. Yeast 2000, 16:57-64.
122. Sims R.J., et al. The C-terminal domain of RNA polymerase II is modified by site-specific methylation. Science 2011, 332:99-103.