Spatial and functional relationships among Pol V-associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome

Genes and Development

Volumn 26, Issue 16, 2012, Pages 1825-1836

  Wierzbicki, Andrzej T ^a   Cocklin, Ross ^b   Mayampurath, Anoop ^c   Lister, Ryan ^d,f   Jordan Rowley, M ^a   Gregory, Brian D ^d,g   Ecker, Joseph R ^d,e   Tang, Haixu ^c   Pikaard, Craig S ^b,e  

^a UNIVERSITY OF MICHIGAN   (United States)

^b INDIANA UNIVERSITY   (United States)

^c INDIANA UNIVERSITY   (United States)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^f UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^g UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

DNA methylation; DNA dependent RNA polymerase; Epigenetics; Gene silencing; RNA directed DNA methylation; Short interfering RNA

Indexed keywords

CYTOSINE; RNA POLYMERASE; RNA POLYMERASE IV; RNA POLYMERASE V; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; BASE PAIRING; BIOGENESIS; CENTROMERE; EPIGENETICS; GENE MUTATION; METHYLATION; NONHUMAN; PRIORITY JOURNAL; RNA SEQUENCE;

AMINO ACID MOTIFS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYTOSINE; DNA METHYLATION; DNA-DIRECTED RNA POLYMERASES; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; MUTATION; RNA, SMALL INTERFERING;

EID: 84865102012     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.197772.112     Document Type: Article

References (39)

1. Cao X, Jacobsen SE. 2002. Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12: 1138-1144
2. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE. 2008. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452: 215-219
3. El-Shami M, Pontier D, Lahmy S, Braun L, Picart C, Vega D Hakimi MA, Jacobsen SE, Cooke R, Lagrange T. 2007. Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAirelated components. Genes Dev 21: 2539-2544.
4. Finnegan EJ, Peacock WJ, Dennis ES. 1996. Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc Natl Acad Sci 93: 8449-8454
5. Gao Z, Liu HL, Daxinger L, Pontes O, He X, Qian W, Lin H, Xie M, Lorkovic ZJ, Zhang S, et al. 2010. An RNA polymerase IIand AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465: 106-109.
6. Haag JR, Pikaard CS. 2011. Multisubunit RNA polymerases IV and V: Purveyors of non-coding RNA for plant gene silencing. Nat Rev Mol Cell Biol 12: 483-492.
7. Herr AJ, Jensen MB, Dalmay T, Baulcombe DC. 2005. RNA polymerase IV directs silencing of endogenous DNA. Science 308: 118-120.
8. Hertz GZ, Stormo GD. 1999. Identifying DNA and protein patterns with statistically significant alignments of multiple sequences. Bioinformatics 15: 563-577
9. Huang L, Jones AM, Searle I, Patel K, Vogler H, Hubner NC Baulcombe DC. 2009. An atypical RNA polymerase involved in RNA silencing shares small subunits with RNA polymerase II. Nat Struct Mol Biol 16: 91-93
10. Huettel B, Kanno T, Daxinger L, Aufsatz W, Matzke AJ, Matzke M. 2006. Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO J 25: 2828-2836.
11. Jensen ST, Liu JS. 2004. BioOptimizer: A Bayesian scoring function approach to motif discovery. Bioinformatics 20: 1557-1564
12. Kanno T, Aufsatz W, Jaligot E, Mette MF, Matzke M, Matzke AJ. 2005a. A SNF2-like protein facilitates dynamic control of DNA methylation. EMBO Rep 6: 649-655
13. Kanno T, Huettel B, Mette MF, Aufsatz W, Jaligot E, Daxinger L Kreil DP, Matzke M, Matzke AJ. 2005b. Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet 37: 761-765
14. Kanno T, Bucher E, Daxinger L, Huettel B, Bohmdorfer G, Gregor W, Kreil DP, Matzke M, Matzke AJ. 2008. A structuralmaintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nat Genet 40: 670-675
15. Law JA, Ausin I, Johnson LM, Vashisht AA, Zhu JK, Wohlschlegel JA, Jacobsen SE. 2010. A protein complex required for polymerase V transcripts and RNA-directed DNA methylation in Arabidopsis. Curr Biol 20: 951-956
16. Li CF, Pontes O, El-Shami M, Henderson IR, Bernatavichute YV Chan SW, Lagrange T, Pikaard CS, Jacobsen SE. 2006. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126: 93-106
17. Lindroth AM, Cao X, Jackson JP, Zilberman D, McCallum CM, Henikoff S, Jacobsen SE. 2001. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292: 2077-2080
18. Lister R, O'Malley RC, Tonti-Filippini J, Gregory BD, Berry CC Millar AH, Ecker JR. 2008. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133: 523-536.
19. Liu X, Brutlag DL, Liu JS. 2001. BioProspector: Discovering conserved DNA motifs in upstream regulatory regions of coexpressed genes. Pac Symp Biocomput 6: 127-138
20. Lu C, Tej SS, Luo S, Haudenschild CD, Meyers BC, Green PJ. 2005. Elucidation of the small RNA component of the transcriptome. Science 309: 1567-1569.
21. Luo J, Hall BD. 2007. A multistep process gave rise to RNA polymerase IV of land plants. J Mol Evol 64: 101-112.
22. Mosher RA, Schwach F, Studholme D, Baulcombe DC. 2008. PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc Natl Acad Sci 105: 3145-3150
23. Olmedo-Monfil V, Duran-Figueroa N, Arteaga-Vazquez M, Demesa-Arevalo E, Autran D, Grimanelli D, Slotkin RK Martienssen RA, Vielle-Calzada J-P. 2010. Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464: 628-632
24. Onodera Y, Haag JR, Ream T, Nunes PC, Pontes O, Pikaard CS. 2005. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120: 613-622
25. Pontes O, Li CF, Nunes PC, Haag J, Ream T, Vitins A, Jacobsen SE, Pikaard CS. 2006. The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 126: 79-92.
26. Pontes O, Costa-Nunes P, Vithayathil P, Pikaard CS. 2009. RNA polymerase V functions in Arabidopsis interphase heterochromatin organization independently of the 24-nt siRNAdirected DNA methylation pathway. Mol Plant 2: 700-710
27. Pontier D, Yahubyan G, Vega D, Bulski A, Saez-Vasquez J Hakimi MA, Lerbs-Mache S, Colot V, Lagrange T. 2005. Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes Dev 19: 2030-2040.
28. Qi Y, Denli AM, Hannon GJ. 2005. Biochemical specialization within Arabidopsis RNA silencing pathways. Mol Cell 19: 421-428.
29. Qi Y, He X, Wang X-J, Kohany O, Jurka J, Hannon GJ. 2006. Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443: 1008-1012
30. Ream TS, Haag JR, Wierzbicki AT, Nicora CD, Norbeck AD, Zhu JK, Hagen G, Guilfoyle TJ, Pasa-Tolic L, Pikaard CS. 2009. Subunit compositions of the RNA-silencing enzymes Pol IV and Pol V reveal their origins as specialized forms of RNA polymerase II. Mol Cell 33: 192-203
31. Ronemus MJ, Galbiati M, Ticknor C, Chen J, Dellaporta SL. 1996. Demethylation-induced developmental pleiotropy in Arabidopsis. Science 273: 654-657.
32. Tucker SL, Reece J, Ream TS, Pikaard CS. 2010. Evolutionary history of plant multisubunit RNA polymerases IV and V: Subunit origins via genome-wide and segmental gene duplications, retrotransposition, and lineage-specific subfunctionalization. Cold Spring Harb Symp Quant Biol 75: 285-297.
33. Wierzbicki AT, Haag JR, Pikaard CS. 2008. Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135: 635-648.
34. Wierzbicki AT, Ream TS, Haag JR, Pikaard CS. 2009. RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat Genet 41: 630-634
35. Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD Zilberman D, Jacobsen SE, Carrington JC. 2004. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2: 642-652
36. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, et al. 2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126: 1189-1201.
37. Zhang X, Henderson IR, Lu C, Green PJ, Jacobsen SE. 2007. Role of RNA polymerase IV in plant small RNA metabolism. Proc Natl Acad Sci 104: 4536-4541
38. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, et al. 2008. Model-based analysis of ChIP-seq (MACS). Genome Biol 9: R137. doi: 10.1186/gb-2008-9-9-r137.
39. Zheng X, Zhu J, Kapoor A, Zhu J-K. 2007. Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing. EMBO J 26: 1691-1701