An Rrp6-like Protein Positively Regulates Noncoding RNA Levels and DNA Methylation in Arabidopsis

Molecular Cell

Volumn 54, Issue 3, 2014, Pages 418-430

  Zhang, Huiming ^a   Tang, Kai ^a   Qian, Weiqiang ^b   Duan, Cheng Guo ^a   Wang, Bangshing ^a   Zhang, Heng ^b   Wang, Pengcheng ^a   Zhu, Xiaohong ^a   Lang, Zhaobo ^a   Yang, Yu ^a,c   Zhu, Jian Kang ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b Chinese Academy of Sciences   (China)

^c LANZHOU UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; ATRRP6L1 PROTEIN; DNA; RNA POLYMERASE; RNA POLYMERASE IV; RNA POLYMERASE V; RRP6 LIKE PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; CHROMATIN; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; EXOSOME; GENE MUTATION; GENETIC SCREENING; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RNA DEGRADATION; RNA PROCESSING; TRANSCRIPTION REGULATION;

ARABIDOPSIS; EUKARYOTA;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMATIN; DNA METHYLATION; DNA-DIRECTED DNA POLYMERASE; EPIGENESIS, GENETIC; EXOSOMES; GENE EXPRESSION REGULATION, PLANT; PROTEIN TRANSPORT; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, PLANT; RNA, SMALL INTERFERING; RNA, UNTRANSLATED;

EID: 84899910150     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.03.019     Document Type: Article

References (45)

1. Assenholt J., Mouaikel J., Andersen K.R., Brodersen D.E., Libri D., Jensen T.H. Exonucleolysis is required for nuclear mRNA quality control in yeast THO mutants. RNA 2008, 14:2305-2313.
2. Bousquet-Antonelli C., Presutti C., Tollervey D. Identification of a regulated pathway for nuclear pre-mRNA turnover. Cell 2000, 102:765-775.
3. Butler J.S., Mitchell P. Rrp6, rrp47 and cofactors of the nuclear exosome. Adv. Exp. Med. Biol. 2011, 702:91-104.
4. Cao X., Jacobsen S.E. Role of the arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr. Biol. 2002, 12:1138-1144.
5. Chekanova J.A., Gregory B.D., Reverdatto S.V., Chen H., Kumar R., Hooker T., Yazaki J., Li P., Skiba N., Peng Q., et al. Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 2007, 131:1340-1353.
6. de Almeida S.F., García-Sacristán A., Custódio N., Carmo-Fonseca M. A link between nuclear RNA surveillance, the human exosome and RNApolymerase II transcriptional termination. Nucleic Acids Res. 2010, 38:8015-8026.
7. Dunoyer P., Brosnan C.A., Schott G., Wang Y., Jay F., Alioua A., Himber C., Voinnet O. An endogenous, systemic RNAi pathway in plants. EMBO J. 2010, 29:1699-1712.
8. Eberle A.B., Hessle V., Helbig R., Dantoft W., Gimber N., Visa N. Splice-site mutations cause Rrp6-mediated nuclear retention of the unspliced RNAs and transcriptional down-regulation of the splicing-defective genes. PLoS ONE 2010, 5:e11540.
9. Girard C., Will C.L., Peng J., Makarov E.M., Kastner B., Lemm I., Urlaub H., Hartmuth K., Lührmann R. Post-transcriptional spliceosomes are retained in nuclear speckles until splicing completion. Nat Commun 2012, 3:994.
10. Haag J.R., Ream T.S., Marasco M., Nicora C.D., Norbeck A.D., Pasa-Tolic L., Pikaard C.S. Invitro 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.
11. Henderson I.R., Jacobsen S.E. Epigenetic inheritance in plants. Nature 2007, 447:418-424.
12. Hessle V., von Euler A., González de Valdivia E., Visa N. Rrp6 is recruited to transcribed genes and accompanies the spliced mRNA to the nuclear pore. RNA 2012, 18:1466-1474.
13. Hilleren P., McCarthy T., Rosbash M., Parker R., Jensen T.H. Quality control of mRNA 3'-end processing is linked to the nuclear exosome. Nature 2001, 413:538-542.
14. Ito H., Gaubert H., Bucher E., Mirouze M., Vaillant I., Paszkowski J. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 2011, 472:115-119.
15. Jasencakova Z., Meister A., Walter J., Turner B.M., Schubert I. Histone H4 acetylation of euchromatin and heterochromatin is cell cycle dependent and correlated with replication rather than with transcription. Plant Cell 2000, 12:2087-2100.
16. Jensen T.H., Patricio K., McCarthy T., Rosbash M. A block to mRNA nuclear export in S. cerevisiae leads to hyperadenylation of transcripts that accumulate at the site of transcription. Mol. Cell 2001, 7:887-898.
17. Kadaba S., Krueger A., Trice T., Krecic A.M., Hinnebusch A.G., Anderson J. Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes Dev. 2004, 18:1227-1240.
18. Kallehauge T.B., Robert M.C., Bertrand E., Jensen T.H. Nuclear retention prevents premature cytoplasmic appearance of mRNA. Mol. Cell 2012, 48:145-152.
19. Kumakura N., Takeda A., Fujioka Y., Motose H., Takano R., Watanabe Y. SGS3 and RDR6 interact and colocalize in cytoplasmic SGS3/RDR6-bodies. FEBS Lett. 2009, 583:1261-1266.
20. Lange H., Holec S., Cognat V., Pieuchot L., Le Ret M., Canaday J., Gagliardi D. Degradation of a polyadenylated rRNA maturation by-product involves one of the three RRP6-like proteins in Arabidopsis thaliana. Mol. Cell. Biol. 2008, 28:3038-3044.
21. Law J.A., Jacobsen S.E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 2010, 11:204-220.
22. Law J.A., Vashisht A.A., Wohlschlegel J.A., Jacobsen S.E. SHH1, a homeodomain protein required for DNA methylation, as well as RDR2, RDM4, and chromatin remodeling factors, associate with RNA polymerase IV. PLoS Genet. 2011, 7:e1002195.
23. Matzke M., Kanno T., Daxinger L., Huettel B., Matzke A.J. RNA-mediated chromatin-based silencing in plants. Curr. Opin. Cell Biol. 2009, 21:367-376.
24. Mosher R.A., Schwach F., Studholme D., Baulcombe D.C. PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc. Natl. Acad. Sci. USA 2008, 105:3145-3150.
25. Neil H., Malabat C., d'Aubenton-Carafa Y., Xu Z., Steinmetz L.M., Jacquier A. Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature 2009, 457:1038-1042.
26. Pandya-Jones A., Black D.L. Co-transcriptional splicing of constitutive and alternative exons. RNA 2009, 15:1896-1908.
27. Phillips S., Butler J.S. Contribution of domain structure to the RNA 3' end processing and degradation functions of the nuclear exosome subunit Rrp6p. RNA 2003, 9:1098-1107.
28. Pikaard C.S., Haag J.R., Pontes O.M., Blevins T., Cocklin R. A transcription fork model for Pol IV and Pol V-dependent RNA-directed DNA methylation. Cold Spring Harb. Symp. Quant. Biol. 2012, 77:205-212.
29. Preker P., Nielsen J., Kammler S., Lykke-Andersen S., Christensen M.S., Mapendano C.K., Schierup M.H., Jensen T.H. RNA exosome depletion reveals transcription upstream of active human promoters. Science 2008, 322:1851-1854.
30. Qian W., Miki D., Zhang H., Liu Y., Zhang X., Tang K., Kan Y., La H., Li X., Li S., et al. A histone acetyltransferase regulates active DNA demethylation in Arabidopsis. Science 2012, 336:1445-1448.
31. Rougemaille M., Gudipati R.K., Olesen J.R., Thomsen R., Seraphin B., Libri D., Jensen T.H. Dissecting mechanisms of nuclear mRNA surveillance in THO/sub2 complex mutants. EMBO J. 2007, 26:2317-2326.
32. Schmid M., Jensen T.H. Quality control of mRNP in the nucleus. Chromosoma 2008, 117:419-429.
33. Shin J.H., Wang H.L., Lee J., Dinwiddie B.L., Belostotsky D.A., Chekanova J.A. The role of the Arabidopsis Exosome in siRNA-independent silencing of heterochromatic loci. PLoS Genet. 2013, 9:e1003411.
34. Torchet C., Bousquet-Antonelli C., Milligan L., Thompson E., Kufel J., Tollervey D. Processing of 3'-extended read-through transcripts by the exosome can generate functional mRNAs. Mol. Cell 2002, 9:1285-1296.
35. West S., Proudfoot N.J., Dye M.J. Molecular dissection of mammalian RNA polymerase II transcriptional termination. Mol. Cell 2008, 29:600-610.
36. Wierzbicki A.T., Haag J.R., Pikaard C.S. Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 2008, 135:635-648.
37. Wierzbicki A.T., Cocklin R., Mayampurath A., Lister R., Rowley M.J., Gregory B.D., Ecker J.R., Tang H., Pikaard C.S. Spatial and functional relationships among Pol V-associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome. Genes Dev. 2012, 26:1825-1836.
38. Xu Z., Wei W., Gagneur J., Perocchi F., Clauder-Münster S., Camblong J., Guffanti E., Stutz F., Huber W., Steinmetz L.M. Bidirectional promoters generate pervasive transcription in yeast. Nature 2009, 457:1033-1037.
39. Yelina N.E., Smith L.M., Jones A.M., Patel K., Kelly K.A., Baulcombe D.C. Putative Arabidopsis THO/TREX mRNA export complex is involved in transgene and endogenous siRNA biosynthesis. Proc. Natl. Acad. Sci. USA 2010, 107:13948-13953.
40. Zemach A., Kim M.Y., Hsieh P.H., Coleman-Derr D., Eshed-Williams L., Thao K., Harmer S.L., Zilberman D. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 2013, 153:193-205.
41. Zhang H., Zhu J.K. RNA-directed DNA methylation. Curr. Opin. Plant Biol. 2011, 14:142-147.
42. Zhang X., Yazaki J., Sundaresan A., Cokus S., Chan S.W., Chen H., Henderson I.R., Shinn P., Pellegrini M., Jacobsen S.E., Ecker J.R. Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 2006, 126:1189-1201.
43. Zhang X., Henderson I.R., Lu C., Green P.J., Jacobsen S.E. Role of RNA polymerase IV in plant small RNA metabolism. Proc. Natl. Acad. Sci. USA 2007, 104:4536-4541.
44. Zheng B., Wang Z., Li S., Yu B., Liu J.Y., Chen X. Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev. 2009, 23:2850-2860.
45. Zhong X., Hale C.J., Law J.A., Johnson L.M., Feng S., Tu A., Jacobsen S.E. DDR complex facilitates global association of RNA polymerase V to promoters and evolutionarily young transposons. Nat. Struct. Mol. Biol. 2012, 19:870-875.