Subunit Compositions of the RNA-silencing Enzymes Pol IV and Pol V Reveal Their Origins As Specialized Forms of RNA Polymerase II

Overview

Journal Mol Cell

Publisher Cell Press

Specialty Cell Biology

Date 2008 Dec 27

PMID 19110459

Citations 143

Authors

Thomas S Ream

Jeremy R Haag

Andrzej T Wierzbicki

Carrie D Nicora

Angela D Norbeck

Jian-Kang Zhu

Gretchen Hagen

Thomas J Guilfoyle

Ljiljana Pasa-Tolic

Craig S Pikaard

Affiliations

Soon will be listed here.

Abstract

In addition to RNA polymerases I, II, and III, the essential RNA polymerases present in all eukaryotes, plants have two additional nuclear RNA polymerases, abbreviated as Pol IV and Pol V, that play nonredundant roles in siRNA-directed DNA methylation and gene silencing. We show that Arabidopsis Pol IV and Pol V are composed of subunits that are paralogous or identical to the 12 subunits of Pol II. Four subunits of Pol IV are distinct from their Pol II paralogs, six subunits of Pol V are distinct from their Pol II paralogs, and four subunits differ between Pol IV and Pol V. Importantly, the subunit differences occur in key positions relative to the template entry and RNA exit paths. Our findings support the hypothesis that Pol IV and Pol V are Pol II-like enzymes that evolved specialized roles in the production of noncoding transcripts for RNA silencing and genome defense.

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References

Rosso M, Li Y, Strizhov N, Reiss B, Dekker K, Weisshaar B . An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol. 2004; 53(1-2):247-59. DOI: 10.1023/B:PLAN.0000009297.37235.4a. View

Pontier D, Yahubyan G, Vega D, Bulski A, Saez-Vasquez J, Hakimi M . Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes Dev. 2005; 19(17):2030-40. PMC: 1199573. DOI: 10.1101/gad.348405. View

Irvine D, Zaratiegui M, Tolia N, Goto D, Chitwood D, Vaughn M . Argonaute slicing is required for heterochromatic silencing and spreading. Science. 2006; 313(5790):1134-7. DOI: 10.1126/science.1128813. View

Alonso J, Stepanova A, Leisse T, Kim C, Chen H, Shinn P . Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 2003; 301(5633):653-7. DOI: 10.1126/science.1086391. View

Kato H, Goto D, Martienssen R, Urano T, Furukawa K, Murakami Y . RNA polymerase II is required for RNAi-dependent heterochromatin assembly. Science. 2005; 309(5733):467-9. DOI: 10.1126/science.1114955. View

Larkin R, Guilfoyle T . Two small subunits in Arabidopsis RNA polymerase II are related to yeast RPB4 and RPB7 and interact with one another. J Biol Chem. 1998; 273(10):5631-7. DOI: 10.1074/jbc.273.10.5631. View

Earley K, Haag J, Pontes O, Opper K, Juehne T, Song K . Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 2006; 45(4):616-29. DOI: 10.1111/j.1365-313X.2005.02617.x. View

Schramm L, Hernandez N . Recruitment of RNA polymerase III to its target promoters. Genes Dev. 2002; 16(20):2593-620. DOI: 10.1101/gad.1018902. View

Dunoyer P, Himber C, Ruiz-Ferrer V, Alioua A, Voinnet O . Intra- and intercellular RNA interference in Arabidopsis thaliana requires components of the microRNA and heterochromatic silencing pathways. Nat Genet. 2007; 39(7):848-56. DOI: 10.1038/ng2081. View

10.

Hamilton A, Voinnet O, Chappell L, Baulcombe D . Two classes of short interfering RNA in RNA silencing. EMBO J. 2002; 21(17):4671-9. PMC: 125409. DOI: 10.1093/emboj/cdf464. View

11.

Myouga F, Tsuchimoto S, Noma K, Ohtsubo H, Ohtsubo E . Identification and structural analysis of SINE elements in the Arabidopsis thaliana genome. Genes Genet Syst. 2001; 76(3):169-79. DOI: 10.1266/ggs.76.169. View

12.

Onodera Y, Haag J, Ream T, Costa Nunes P, Pontes O, Pikaard C . Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell. 2005; 120(5):613-22. DOI: 10.1016/j.cell.2005.02.007. View

13.

Saez-Vasquez J, Pikaard C . Extensive purification of a putative RNA polymerase I holoenzyme from plants that accurately initiates rRNA gene transcription in vitro. Proc Natl Acad Sci U S A. 1997; 94(22):11869-74. PMC: 23640. DOI: 10.1073/pnas.94.22.11869. View

14.

Baumberger N, Baulcombe D . Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci U S A. 2005; 102(33):11928-33. PMC: 1182554. DOI: 10.1073/pnas.0505461102. View

15.

Gnatt A, Cramer P, Fu J, Bushnell D, Kornberg R . Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 A resolution. Science. 2001; 292(5523):1876-82. DOI: 10.1126/science.1059495. View

16.

Cramer P . RNA polymerase II structure: from core to functional complexes. Curr Opin Genet Dev. 2004; 14(2):218-26. DOI: 10.1016/j.gde.2004.01.003. View

17.

Borsani O, Zhu J, Verslues P, Sunkar R, Zhu J . Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell. 2005; 123(7):1279-91. PMC: 3137516. DOI: 10.1016/j.cell.2005.11.035. View

18.

Sessions A, Burke E, Presting G, Aux G, McElver J, Patton D . A high-throughput Arabidopsis reverse genetics system. Plant Cell. 2002; 14(12):2985-94. PMC: 151197. DOI: 10.1105/tpc.004630. View

19.

Cheong J, Yi M, Lin Y, Murakami S . Human RPB5, a subunit shared by eukaryotic nuclear RNA polymerases, binds human hepatitis B virus X protein and may play a role in X transactivation. EMBO J. 1995; 14(1):143-50. PMC: 398061. DOI: 10.1002/j.1460-2075.1995.tb06984.x. View

20.

Woychik N, Hampsey M . The RNA polymerase II machinery: structure illuminates function. Cell. 2002; 108(4):453-63. DOI: 10.1016/s0092-8674(02)00646-3. View