Arabidopsis double-stranded RNA binding protein DRB3 participates in methylation-mediated defense against geminiviruses

Journal of Virology

Volumn 88, Issue 5, 2014, Pages 2611-2622

  Raja, Priya ^a,b   Jackel, Jamie N ^a   Li, Sizhun ^a   Heard, Isaac M ^a   Bisaro, David M ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 4 PROTEIN; ARGONAUTE PROTEIN; DICER; DOUBLE STRANDED RNA; DOUBLE STRANDED RNA BINDING PROTEIN 3; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CHROMATIN; CONTROLLED STUDY; DNA METHYLATION; GEMINIVIRUS; GENETIC EPIGENESIS; IMMUNOPRECIPITATION; NONHUMAN; PLANT DEFENSE; PLANT MICROORGANISM INTERACTION; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; VIRUS GENE; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ARGONAUTE PROTEINS; DISEASE RESISTANCE; DNA METHYLATION; GEMINIVIRIDAE; GENOME, VIRAL; METHYLATION; MUTATION; PHENOTYPE; PLANT DISEASES; PROTEIN BINDING; RIBONUCLEASE III; RNA, DOUBLE-STRANDED; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS;

EID: 84896727170     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02305-13     Document Type: Article

References (71)

1. Baulcombe DC. 2004. RNA silencing in plants. Nature 431:356-363. http://dx.doi.org/10.1038/nature02874.
2. Brodersen P, Voinnet O. 2006. The diversity of RNA silencing pathways in plants. Trends Genet. 22:268-280. http://dx.doi.org/10.1016/j.tig.2006 .03.003.
3. Vaucheret H. 2006. Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev. 20:759-771. http://dx.doi.org /10.1101/gad.1410506.
4. Henderson IR, Jacobsen SE. 2007. Epigenetic inheritance in plants. Nature 447:418-424. http://dx.doi.org/10.1038/nature05917.
5. Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJM. 2009. RNA-mediated chromatin-based silencing in plants. Curr. Opin. Cell Biol. 21:367-376. http://dx.doi.org/10.1016/j.ceb.2009.01.025.
6. Law JA, Jacobsen SE. 2010. Establishing, maintaining, and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11: 204-220. http://dx.doi.org/10.1038/nrg2719.
7. Ding S-W, Voinnet O. 2007. Antiviral immunity directed by small RNAs. Cell 130:413-426. http://dx.doi.org/10.1016/j.cell.2007.07.039.
8. Mlotshwa S, Pruss GJ, Vance V. 2008. Small RNAs in viral infection and host defense. Trends Plant Sci. 13:375-382. http://dx.doi.org/10.1016/j .tplants.2008.04.009.
9. Ruiz-Ferrer V, Voinnet O. 2009. Roles of plant small RNAs in biotic stress responses. Annu. Rev. Plant Biol. 60:485-510. http://dx.doi.org/10.1146 /annurev.arplant.043008.092111.
10. Saunders LR, Barber GN. 2003. The dsRNA binding protein family: critical roles, diverse cellular functions. FASEB J. 17:961-983. http://dx .doi.org/10.1096/fj.02-0958rev.
11. Chang K-Y, Ramos A. 2005. The double-stranded RNA-binding motif, a versatile macromolecular docking platform. FEBS J. 272:2109-2117. http: //dx.doi.org/10.1111/j.1742-4658.2005.04652.x.
12. Hiraguri A, Itoh R, Kondo N, Nomura Y, Aizawa D, Murai Y, Koiwa H, Seki M, Shinozaki K, Fukuhara T. 2005. Specific interacions between Dicer-like proteins and HYL1/DRB-family dsRNA-binding proteins in Arabidopsis thaliana. Plant Mol. Biol. 57:173-188. http://dx.doi.org/10 .1007/s11103-004-6853-5.
13. Tabara H, Yigit E, Siomi H, Mello C. 2002. The dsRNA binding protein RDE-4 interacts with RDE-1, DCR-1, and a DExH-box helicase to direct RNAi in C. elegans. Cell 109:861-871. http://dx.doi.org/10.1016/S0092 -8674(02)00793-6.
14. Liu Q, Rand TA, Kalidas S, Du F, Kim H-E, Smith DP, Wang X. 2003. R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway. Science 301:1921-1925. http://dx.doi.org/10.1126/science .1088710.
15. Jiang F, Ye X, Liu X, Fincher L, McKearin D, Liu Q. 2005. Dicer-1 and R3D1-L catalyze microRNA maturation in Drosophila. Genes Dev. 19: 1674-1679. http://dx.doi.org/10.1101/gad.1334005.
16. Han M-H, Goud S, Song L, Federoff N. 2004. The Arabidopsis doublestranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc. Natl. Acad. Sci. U. S. A. 101:1093-1098. http://dx .doi.org/10.1073/pnas.0307969100.
17. Vasquez F, Gasciolli V, Crete P, Vaucheret H. 2004. The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr. Biol. 14:348-351. http://dx.doi.org/10.1016/j.cub.2004.01.035.
18. Curtin SJ, Watson JM, Smith NA, Eamens AL, Blanchard CL, Waterhouse PM. 2008. The roles of plant dsRNA-binding proteins in RNAi-like pathways. FEBS Lett. 582:2753-2760. http://dx.doi.org/10.1016/j.febslet .2008.07.004.
19. Eamens AL, Smith NA, Curtin S, Wang M-B, Waterhouse PM. 2009. The Arabidopsis thaliana double-stranded RNA binding protein DRB1 directs guide strand selection from microRNA duplexes. RNA 15:2219-2235. http://dx.doi.org/10.1261/rna.1646909.
20. Eamens AL, Kim KW, Curtin SJ, Waterhouse PM. 2012. DRB2 is required for microRNA biogenesis in Arabidopsis thaliana. PLoS One 7:e35933. http://dx.doi.org/10.1371/journal.pone.0035933.
21. Eamens AL, Wook KK, Waterhouse PM. 2012. DRB2, DRB3 and DRB5 function in a non-canonical microRNA pathway in Arabidopsis thaliana. Plant Signal. Behav. 7:1224-1229. http://dx.doi.org/10.4161/psb.21518.
22. Adenot X, Elmayan T, Lauressergues D, Boutet S, Bouche N, Gasciolli V, Vaucheret H. 2006. DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr. Biol. 16:927-932. http://dx .doi.org/10.1016/j.cub.2006.03.035.
23. Nakazawa Y, Hiraguri A, Moriyama H, Fukuhara T. 2007. The dsRNAbinding protein DRB4 interacts with the Dicer-like protein DCL4 in vivo and functions in the trans-acting siRNA pathway. Plant Mol. Biol. 63:777-785. http://dx.doi.org/10.1007/s11103-006-9125-8.
24. Qu F, Ye X, Morris TJ. 2008. Arabidopsis DRB4, AGO1, AGO7, and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. Proc. Natl. Acad. Sci. U. S. A. 105:14732-14737. http://dx.doi.org/10.1073/pnas.0805760105.
25. Haas G, Azevado J, Moissard G, Geldreich A, Himber C, Bureau M, Fukuhara T, Keller M, Voinnet O. 2008. Nuclear import of CaMV P6 is required for infection and suppression of the RNA silencing factor DRB4. EMBO J. 27:2102-2112. http://dx.doi.org/10.1038/emboj.2008.129.
26. Eamens AL, Curtin SJ, Waterhouse PM. 2011. The Arabidopsis thaliana double-stranded RNA binding (DRB) domain protein family, p 385-403. In Erdmann VA, Barciszewski J. (ed), Noncoding RNAs in plants. Springer, Berlin, Germany.
27. Pelissier T, Clavel M, Chaparro C, Pouch-Pelissier M-N, Vaucharet H, Deragon J-M. 2011. Double-stranded RNA binding proteins DRB2 and DRB4 have an antagonistic impact on polymerase IV-dependent siRNA levels in Arabidopsis. RNA 17:1502-1510. http://dx.doi.org/10.1261/rna .2680711.
28. Rojas MR, Hagen C, Lucas WJ, Gilbertson RL. 2005. Exploiting chinks in the plant's armor: evolution and emergence of geminiviruses. Annu. Rev. Phytopathol. 43:361-394. http://dx.doi.org/10.1146/annurev.phyto .43.040204.135939.
29. Jeske H. 2009. Geminiviruses. Curr. Top. Immunol. Microbiol. 331:185-226.
30. Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S. 2013. Geminiviruses: masters at redirecting and reprogramming plant processes. Nat. Rev. Microbiol. 11:777-788. http://dx.doi.org/10.1038 /nrmicro3117.
31. Vanitharani R, Chellappan P, Fauquet CM. 2005. Geminiviruses and RNA silencing. Trends Plant Sci. 10:144-151. http://dx.doi.org/10.1016/j .tplants.2005.01.005.
32. Bisaro DM. 2006. Silencing suppression by geminivirus proteins. Virology 344:158-168. http://dx.doi.org/10.1016/j.virol.2005.09.041.
33. Raja P, Sanville BC, Buchmann RC, Bisaro DM. 2008. Viral genome methylation as an epigenetic defense against geminiviruses. J. Virol. 82: 8997-9007. http://dx.doi.org/10.1128/JVI.00719-08.
34. Buchmann RC, Asad S, Wolf JN, Mohannath G, Bisaro DM. 2009. Geminivirus AL2 and L2 proteins suppress transcriptional gene silencing and cause genome-wide reductions in cytosine methylation. J. Virol. 83: 5005-5013. http://dx.doi.org/10.1128/JVI.01771-08.
35. Raja P, Wolf JN, Bisaro DM. 2010. RNA silencing directed against geminiviruses: post-transcriptional and epigenetic components. Biochim. Biophys. Acta 1799:337-351. http://dx.doi.org/10.1016/j.bbagrm.2010.01 .004.
36. Yang X, Xie Y, Raja P, Li S, Wolf JN, Shen Q, Bisaro DM, Zhou X. 2011. Suppression of methylation-mediated transcriptional gene silencing by C1-SAHH protein interaction during geminivirus-betasatellite infection. PLoS Pathog. 7:e1002329. http://dx.doi.org/10.1371/journal.ppat .1002329.
37. Lisch D. 2009. Epigenetic regulation of transposable elements in plants. Annu. Rev. Plant Biol. 60:43-66. http://dx.doi.org/10.1146/annurev .arplant.59.032607.092744.
38. 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:e104. http://dx .doi.org/10.1371/journal.pbio.0020104.
39. Zilberman D, Cao X, Jacobsen SE. 2003. Argonaute4 control of locusspecific siRNA accumulation and DNA and histone methylation. Science 299:716-719. http://dx.doi.org/10.1126/science.1079695.
40. Hormuzdi SG, Bisaro DM. 1995. Genetic analysis of beet curly top virus: examination of the roles of L2 and L3 genes in viral pathogenesis. Virology 206:1044-1054. http://dx.doi.org/10.1006/viro.1995.1027.
41. Hu C-D, Chinenov Y, Kerppola TK. 2002. Visualization of interactions among bZIP and Rel family proteins using bimolecular fluorescence complementation. Mol. Cell 9:789-798. http://dx.doi.org/10.1016/S1097 -2765(02)00496-3.
42. Yang X, Baliji S, Buchmann RC, Wang H, Lindbo JA, Sunter G, Bisaro DM. 2007. Functional modulation of the geminivirus AL2 transcription factor and silencing suppressor by self-interaction. J. Virol. 81:11972-11981. http://dx.doi.org/10.1128/JVI.00617-07.
43. Wang H, Buckley KJ, Yang X, Buchmann RC, Bisaro DM. 2005. Adenosine kinase inhibition and suppression of RNA silencing by geminivirus AL2 and L2 proteins. J. Virol. 79:7410-7418. http://dx.doi.org/10 .1128/JVI.79.12.7410-7418.2005.
44. Chakrabarty R, Banerjee R, Chung S-M, Farman M, Citovsky V, Hogenhout SA, Tzfira T, Goodin M. 2007. pSITE vectors for stable integration or transient expression of autofluorescent protein fusions in plants: probing Nicotiana benthamiana-virus interactions. Mol. Plant Microbe Interact. 20:740-750. http://dx.doi.org/10.1094/MPMI-20-7-0740.
45. Wang H, Hao L, Shung C-Y, Sunter G, Bisaro DM. 2003. Adenosine kinase is inactivated by geminivirus AL2 and L2 proteins. Plant Cell 15: 3020-3032. http://dx.doi.org/10.1105/tpc.015180.
46. 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. http://dx.doi.org/10.1016/j.cell.2006.05.031.
47. Lindbo JA. 2007. TRBO: a high-efficiency tobacco mosiac virus RNAbased overexpression vector. Plant Physiol. 145:1232-1240. http://dx.doi .org/10.1104/pp.107.106377.
48. Frommer M, McDonald LE, Millar DS, Collis CM, Watt F, Grigg GW, Malloy PW, Paul CL. 1992. A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc. Natl. Acad. Sci. U. S. A. 89:1827-1831. http://dx.doi.org/10.1073 /pnas.89.5.1827.
49. Gruntman E, Qi Y, Slotkin RK, Roeder T, Martienssen RA, Sachidan-andam R. 2008. Kismeth: analyzer of plant methylation states through bisulfite sequencing. BMC Bioinformatics 9:371. http://dx.doi.org/10 .1186/1471-2105-9-371.
50. Hagen C, Rojas MR, Kon T, Gilbertson RL. 2008. Recovery from Cucurbit leaf crumple virus (family Geminiviridae, genus Begomovirus) infection is an adaptive antiviral response associated with changes in small viral RNAs. Phytopathology 98:1029-1037. http://dx.doi.org/10.1094/PHYTO -98-9-1029.
51. Rodriguez-Negrete EA, Carrillo-Trip J, Rivera-Bustamante RF. 2009. RNA silencing against geminivirus: complementary action of posttranscriptional gene silencing and transcriptional gene silencing in host recovery. J. Virol. 83:1332-1340. http://dx.doi.org/10.1128/JVI.01474-08.
52. Brough CL, Gardiner WE, Inamdar N, Zhang XY, Ehrlich M, Bisaro DM. 1992. DNA methylation inhibits propagation of tomato golden mosaic virus DNA in transfected protoplasts. Plant Mol. Biol. 18:703-712. http://dx.doi.org/10.1007/BF00020012.
53. Ermak G, Paszkowski U, Wohlmuth M, Scheid OM, Paszkowski J. 1993. Cytosine methylation inhibits replication of African cassava mosaic virus by two distinct mechanisms. Nucleic Acids Res. 21:3445-3450. http://dx .doi.org/10.1093/nar/21.15.3445.
54. Gasciolli V, Mallory AC, Bartel DP, Vaucheret H. 2005. Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr. Biol. 15:1494-1500. http://dx.doi .org/10.1016/j.cub.2005.07.024.
55. Henderson IR, Zhang X, Lu C, Johnson L, Meyers BC, Green PJ, Jacobsen SE. 2006. Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nat. Genet. 38:721-725. http://dx.doi.org/10.1038/ng1804.
56. Blevins T, Rajeswaran R, Shivaprasad PV, Beknazariants D, Si-Ammour A, Park H-S, Vazquez F, Robertson D, Meins F, Hohn T, Pooggin MM. 2006. Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res. 34:6233-6246. http: //dx.doi.org/10.1093/nar/gkl886.
57. Bouche N, Lauressergues D, Gasciolli V, Vaucheret H. 2006. An antagonistic function for Arabidopsis DCL2 in development and a new function for DCL4 in generating viral siRNAs. EMBO J. 25:3347-3356. http://dx .doi.org/10.1038/sj.emboj.7601217.
58. Deleris A, Gallego-Bartolome J, Bao J, Kasschau K, Carrington JC, Voinnet O. 2006. Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313:68-71. http://dx.doi.org/10 .1126/science.1128214.
59. Cañizares MC, Lozano-Durán R, Canto T, Bejarano ER, Bisaro DM, Navas-Castillo J, Moriones E. 2013. Effects of crinivirus coat proteininteracting plant protein SAHH on post-transcriptional RNA silencing and its suppression. Mol. Plant Microbe Interact. 26:1004-1015. http://dx .doi.org/10.1094/MPMI-02-13-0037-R.
60. Li CF, Pontes O, El-Shami M, Henderson IR, Bernatavichute YV, Chan SW-L, Lagrange T, Pikaard CS, Jacobsen SE. 2006. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126:93-106. http://dx.doi.org/10.1016/j.cell.2006 .05.032.
61. Li CF, Henderson IR, Song L, Federoff N, Lagrange T, Jacobsen SE. 2008. Dynamic regulation of ARGONAUTE4 within multiple nuclear bodies in Arabidopsis thaliana. PLoS Genet. 4:e27. http://dx.doi.org/10 .1371/journal.pgen.0040027.
62. Akbergenov R, Si-Ammour A, Blevins T, Amin I, Kutter C, Vanderschuren H, Zhang P, Gruissem W, Meins F, Jr, Hohn T, Pooggin MM. 2006. Molecular characterization of geminivirus-derived small RNAs in different plant species. Nucleic Acids Res. 34:462-471. http://dx.doi.org /10.1093/nar/gkj447.
63. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P. 2008. Genevestigator V3: a reference expression database for meta-analysis of transcriptomes. Adv. Bioinformatics 2008:420747. http://dx.doi.org/10.1155/2008/420747.
64. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pelligrini M, Jacobsen SE. 2008. Shotgun bisuphite sequencing of the Arabidopsis genome revealsDNAmethylation patterning. Nature 452:215-219. http://dx.doi.org/10.1038/nature06745.
65. 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. http://dx.doi.org/10.1016/j .cell.2008.03.029.
66. Zemach A, Kim MY, Coleman-Derr D, Eshed-Williams L, Thao K, Harmer S, Zilberman D. 2013. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153:193-205. http://dx.doi.org/10.1016/j.cell.2013.02 .033.
67. Nuthikattu S, McCue AD, Panda K, Fultz D, DeFraia C, Thomas EN, Slotkin RK. 2013. The initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21-22 nucleotide small interfering RNAs. Plant Physiol. 162:116-131. http://dx.doi.org/10.1104/pp.113 .216481.
68. Jeske H, Lutgemeier M, Preiss W. 2001. DNA forms indicate rolling circle and recombination-dependent replication of Abutilon mosaic virus. EMBO J. 20:6158-6167. http://dx.doi.org/10.1093/emboj/20.21.6158.
69. Preiss W, Jeske H. 2003. Multitasking in replication is common among geminiviruses. J. Virol. 77:2972-2980. http://dx.doi.org/10.1128/JVI.77.5 .2972-2980.2003.
70. Paprotka T, Deuschle K, Metzler V, Jeske H. 2011. Conformationselective methylation of geminivirus DNA. J. Virol. 85:12001-12012. http: //dx.doi.org/10.1128/JVI.05567-11.
71. Zilberman D, Cao X, Johansen LK, Xie Z, Carrington JC, Jacobsen SE. 2004. Role of Arabidopsis ARGONAUTE4 in RNA-directed DNA methylation triggered by inverted repeats. Curr. Biol. 14:1214-1220. http://dx .doi.org/10.1016/j.cub.2004.06.055.