RNA-directed DNA Methylation and Plant Development Require an IWR1-type Transcription Factor

Overview

Journal EMBO Rep

Specialty Molecular Biology

Date 2009 Dec 17

PMID 20010803

Citations 40

Authors

Tatsuo Kanno

Etienne Bucher

Lucia Daxinger

Bruno Huettel

David P Kreil

Frank Breinig

Marc Lind

Manfred J Schmitt

Stacey A Simon

Sai Guna Ranjan Gurazada

Blake C Meyers

Zdravko J Lorkovic

Antonius J M Matzke

Marjori Matzke

Affiliations

Soon will be listed here.

Abstract

RNA-directed DNA methylation (RdDM) in plants requires two RNA polymerase (Pol) II-related RNA polymerases, namely Pol IV and Pol V. A genetic screen designed to reveal factors that are important for RdDM in a developmental context in Arabidopsis identified DEFECTIVE IN MERISTEM SILENCING 4 (DMS4). Unlike other mutants defective in RdDM, dms4 mutants have a pleiotropic developmental phenotype. The DMS4 protein is similar to yeast IWR1 (interacts with RNA polymerase II), a conserved putative transcription factor that interacts with Pol II subunits. The DMS4 complementary DNA partly complements the K1 killer toxin hypersensitivity of a yeast iwr1 mutant, suggesting some functional conservation. In the transgenic system studied, mutations in DMS4 directly or indirectly affect Pol IV-dependent secondary short interfering RNAs, Pol V-mediated RdDM, Pol V-dependent synthesis of intergenic non-coding RNA and expression of many Pol II-driven genes. These data suggest that DMS4 might be a regulatory factor for several RNA polymerases, thus explaining its diverse roles in the plant.

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References

Bies-Etheve N, Pontier D, Lahmy S, Picart C, Vega D, Cooke R . RNA-directed DNA methylation requires an AGO4-interacting member of the SPT5 elongation factor family. EMBO Rep. 2009; 10(6):649-54. PMC: 2711833. DOI: 10.1038/embor.2009.31. View

Pikaard C, Haag J, Ream T, Wierzbicki A . Roles of RNA polymerase IV in gene silencing. Trends Plant Sci. 2008; 13(7):390-7. PMC: 2679257. DOI: 10.1016/j.tplants.2008.04.008. View

Ream T, Haag J, Wierzbicki A, Nicora C, Norbeck A, Zhu J . Subunit compositions of the RNA-silencing enzymes Pol IV and Pol V reveal their origins as specialized forms of RNA polymerase II. Mol Cell. 2008; 33(2):192-203. PMC: 2946823. DOI: 10.1016/j.molcel.2008.12.015. View

Kanno T, Bucher E, Daxinger L, Huettel B, Bohmdorfer G, Gregor W . A structural-maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nat Genet. 2008; 40(5):670-5. DOI: 10.1038/ng.119. View

Li Z, Barajas D, Panavas T, Herbst D, Nagy P . Cdc34p ubiquitin-conjugating enzyme is a component of the tombusvirus replicase complex and ubiquitinates p33 replication protein. J Virol. 2008; 82(14):6911-26. PMC: 2446948. DOI: 10.1128/JVI.00702-08. View

He X, Hsu Y, Pontes O, Zhu J, Lu J, Bressan R . NRPD4, a protein related to the RPB4 subunit of RNA polymerase II, is a component of RNA polymerases IV and V and is required for RNA-directed DNA methylation. Genes Dev. 2009; 23(3):318-30. PMC: 2648547. DOI: 10.1101/gad.1765209. View

Verdel A, Vavasseur A, Le Gorrec M, Touat-Todeschini L . Common themes in siRNA-mediated epigenetic silencing pathways. Int J Dev Biol. 2009; 53(2-3):245-57. DOI: 10.1387/ijdb.082691av. View

Page N, Gerard-Vincent M, Menard P, Beaulieu M, Azuma M, Dijkgraaf G . A Saccharomyces cerevisiae genome-wide mutant screen for altered sensitivity to K1 killer toxin. Genetics. 2003; 163(3):875-94. PMC: 1462477. DOI: 10.1093/genetics/163.3.875. View

Huang L, Jones A, Searle I, Patel K, Vogler H, Hubner N . An atypical RNA polymerase involved in RNA silencing shares small subunits with RNA polymerase II. Nat Struct Mol Biol. 2008; 16(1):91-3. DOI: 10.1038/nsmb.1539. View

10.

Huettel B, Kanno T, Daxinger L, Aufsatz W, Matzke A, Matzke M . Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO J. 2006; 25(12):2828-36. PMC: 1500864. DOI: 10.1038/sj.emboj.7601150. View

11.

Daxinger L, Kanno T, Bucher E, van der Winden J, Naumann U, Matzke A . A stepwise pathway for biogenesis of 24-nt secondary siRNAs and spreading of DNA methylation. EMBO J. 2008; 28(1):48-57. PMC: 2633084. DOI: 10.1038/emboj.2008.260. View

12.

Peiro-Chova L, Estruch F . The yeast RNA polymerase II-associated factor Iwr1p is involved in the basal and regulated transcription of specific genes. J Biol Chem. 2009; 284(42):28958-67. PMC: 2781442. DOI: 10.1074/jbc.M109.012153. View

13.

He X, Hsu Y, Zhu S, Wierzbicki A, Pontes O, Pikaard C . An effector of RNA-directed DNA methylation in arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell. 2009; 137(3):498-508. PMC: 2700824. DOI: 10.1016/j.cell.2009.04.028. View

14.

Kanno T, Huettel B, Mette M, Aufsatz W, Jaligot E, Daxinger L . Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet. 2005; 37(7):761-5. DOI: 10.1038/ng1580. View

15.

Krogan N, Cagney G, Yu H, Zhong G, Guo X, Ignatchenko A . Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature. 2006; 440(7084):637-43. DOI: 10.1038/nature04670. View

16.

Matzke M, Kanno T, Daxinger L, Huettel B, Matzke A . RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol. 2009; 21(3):367-76. DOI: 10.1016/j.ceb.2009.01.025. View

17.

Aouida M, Page N, Leduc A, Peter M, Ramotar D . A genome-wide screen in Saccharomyces cerevisiae reveals altered transport as a mechanism of resistance to the anticancer drug bleomycin. Cancer Res. 2004; 64(3):1102-9. DOI: 10.1158/0008-5472.can-03-2729. View

18.

Wierzbicki A, Haag J, Pikaard C . Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell. 2008; 135(4):635-48. PMC: 2602798. DOI: 10.1016/j.cell.2008.09.035. View

19.

Collins S, Miller K, Maas N, Roguev A, Fillingham J, Chu C . Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature. 2007; 446(7137):806-10. DOI: 10.1038/nature05649. View

20.

Roguev A, Bandyopadhyay S, Zofall M, Zhang K, Fischer T, Collins S . Conservation and rewiring of functional modules revealed by an epistasis map in fission yeast. Science. 2008; 322(5900):405-10. PMC: 2753251. DOI: 10.1126/science.1162609. View