The protein kinase TOUSLED facilitates RNAi in Arabidopsis

Nucleic Acids Research

Volumn 42, Issue 12, 2014, Pages 7971-7980

  Uddin, Mohammad Nazim ^a   Dunoyer, Patrice ^b   Schott, Gregory ^b   Akhter, Salina ^a   Shi, Chunlin ^a   Lucas, William J ^a,c   Voinnet, Olivier ^b,d   Kim, Jae Yean ^a  

^a Gyeongsang National University   (South Korea)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA; MICRORNA 173; MICRORNA 390; MICRORNA 396; PROTEIN SERINE THREONINE KINASE; SMALL INTERFERING RNA; TOUSLED PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE SILENCING; ILS1 GENE; ILS2 GENE; ILS3 GENE; ILS4 GENE; NONHUMAN; PLANT GENE; PRIORITY JOURNAL; REGULATORY MECHANISM; RNA CLEAVAGE; RNA DEGRADATION; RNA INTERFERENCE; RNA STABILITY; RNA SYNTHESIS; TSL GENE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; PLANTS, GENETICALLY MODIFIED; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; RNA, SMALL UNTRANSLATED; RNA-INDUCED SILENCING COMPLEX;

EID: 84904016029     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku422     Document Type: Article

References (54)

1. Baulcombe, D.C. (2004) RNA silencing in plants. Nature, 431, 356-363.
2. Voinnet, O. (2009) Origin, biogenesis, and activity of plant microRNAs. Cell, 136, 669-687.
3. Chapman, E.J., Carrington, J.C. (2007) Specialization and evolution of endogenous small RNA pathways. Nat. Rev. Genet., 8, 884-896.
4. Baumberger, N., Baulcombe, D.C. (2005) Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl. Acad. Sci. U.S.A., 102, 11928-11933.
5. Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y.Y., Sieburth, L., Voinnet, O. (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science, 320, 1185-1190.
6. Law, J.A., Jacobsen, S.E. (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet., 11, 204-220.
7. Palauqui, J.C., Elmayan, T., Pollien, J.M., Vaucheret, H. (1997) Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J., 16, 4738-4745.
8. Voinnet, O., Vain, P., Angell, S., Baulcombe, D.C. (1998) Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell, 95, 177-187.
9. Dunoyer, P., Schott, G., Himber, C., Meyer, D., Takeda, A., Carrington, J.C., Voinnet, O. (2010) Small RNA duplexes function as mobile silencing signals between plant cells. Science, 328, 912-916.
10. Molnar, A., Melnyk, C.W., Bassett, A., Hardcastle, T.J., Baulcombe, D.C. (2010) Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science, 328, 872-875.
11. Dunoyer, P., Brosnan, C.A., Schott, G., Wang, Y., Jay, F., Aliqua, A., Himber, C., Voinnet, O. (2010) An endogenous, systemic RNAi pathway in plants. EMBO J., 29, 1699-1712.
12. Havelda, Z., Hornyik, C., Crescenzi, A., Burgyan, J. (2003) In situ characterization of Cymbidium ringspot tombusvirus infection-induced posttranscriptional gene silencing in Nicotiana benthamiana. J. Virol., 77, 6082-6086.
13. Chitwood, D.H., Nogueira, F.T.S., Howell, M.D., Montgomery, T.A., Carrington, J.C., Timmermans, M.C.P. (2009) Pattern formation via small RNA mobility. Genes Dev., 23, 549-554.
14. Schwab, R., Maizel, A., Ruiz-Ferrer, V., Gracia, D., Bayer, M., Crespi, M., Voinnet, O., Martienssen, R.A. (2009) Endogenous tasiRNAs mediate non-cell autonomous effects on gene regulation in Arabidopsis thaliana. PLoS One, 4, e5980.
15. Bologna, N.G., Voinnet, O. (2014) The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu. Rev. Plant Biol., 65, 473-503.
16. Dunoyer, P., Himber, C., Ruiz-Ferrer, V., Alioua, A., Voinnet, O. (2007) Intra-and intercellular RNA interference in Arabidopsis thaliana requires components of the microRNA and heterochromatic silencing pathways. Nat. Genet, 39, 848-856.
17. Smith, L.M., Pontes, O., Searle, I., Yelina, N., Yousafzai, F.K., Herr, A.J., Pikaard, C.S., Baulcombe, D.C. (2007) An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell, 19, 1507-1521.
18. Brosnan, C.A., Mitter, N., Christie, M., Smith, N.A., Waterhouse, P.M., Carroll, B.J. (2007) Nuclear gene silencing directs reception of long-distance mRNA silencing in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A., 104, 14741-14746.
19. Boutet, S., Vazquez, F., Liu, J., Béclin, C., Fagard, M., Gratias, A., Morel, J.B., Crété, P., Chen, X., Vaucheret, H. (2003) Arabidopsis HEN1: a genetic link between endogenous miRNA controlling development and siRNA controlling transgene silencing and virus resistance. Curr. Biol., 13, 843-848.
20. Roe, J.L., Rivin, C.J., Sessions, R.A., Feldmann, K.A., Zambryski, P.C. (1993) The TOUSLED gene in A. thaliana encodes a protein kinase homolog that is required for leaf and flower development. Cell, 75, 939-950.
21. Li, J., Yang, Z., Yu, B., Liu, J., Chen, X. (2005) Methylation protects miRNAs and siRNAs from a 3'-end uridylation activity in Arabidopsis. Curr. Biol., 15, 1501-1507.
22. Roe, J.L., Durfee, T., Zupan, J.R., Repetti, P.P., McLean, B.G., Zambryski, P.C. (1997) TOUSLED is a nuclear serine/threonine protein kinase that requires a coiled-coil region for oligomerization and catalytic activity. J. Biol. Chem., 272, 5838-5845.
23. Clough, S.J., Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J., 16, 735-743.
24. Chinnusamy, V., Stevenson, B., Lee, B.H., Zhu, J.K. (2002) Screening for gene regulation mutants by bioluminescence imaging. Sci. STKE, 140, l10.
25. Yu, D., Fan, B., MacFarlane, S.A., Chen, Z. (2003) Analysis of involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. Mol. Plant Microbe Interact., 16, 206-216.
26. Deleris, A., Gallego-Bartolome, J., Bao, J., Kasschau, K.D., Carrington, J.C., Voinnet, O. (2006) Hierarchical action and inhibition of plant dicer-like proteins in antiviral defense. Science, 313, 68-71.
27. Adrian, J., Farrona, S., Reimer, J.J., Albani, M.C., Coupland, G., Turck, F. (2010) Cis-regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis. Plant Cell, 22, 1425-1440.
28. Dunoyer, P., Lecellier, C.H., Parizotto, E.A., Himber, C., Voinnet, O. (2004) Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell, 16, 1235-1250.
29. Vargason, J.M., Szittya, G., Burgyan, J., Hall, T.M. (2003) Size selective recognition of siRNA by an RNA silencing suppressor. Cell, 115, 799-811.
30. Dunoyer, P., Himber, C., Voinnet, O. (2005) DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat. Genet., 37, 1356-1360.
31. Moissiard, G., Voinnet, O. (2006) RNA silencing of host transcripts by cauliflower mosaic virus requires coordinated action of the four Arabidopsis Dicer-like proteins. Proc. Natl. Acad. Sci. U.S.A., 103, 19593-19598.
32. Himber, C., Dunoyer, P., Moissiard, G., Ritzenthaler, C., Voinnet, O. (2003) Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO J., 22, 4523-4533.
33. Christie, M., Croft, L.J., Carroll, B.J. (2011) Intron splicing suppresses RNA silencing in Arabidopsis. Plant J., 68, 159-167.
34. Wang, Y., Liu, J., Xia, R., Wang, J., Shen, J., Cao, R., Hong, X., Zhu, J.K., Gong, Z. (2007) The protein kinase TOUSLED is required for maintenance of transcriptional gene silencing in Arabidopsis. EMBO Rep., 8, 77-83.
35. Donaire, L., Barajas, D., Martinez-Garcia, B., Martinez-Priego, L., Pagán, I., Llave, C. (2008) Structural and genetic requirements for the biogenesis of Tobacco rattle virus-derived small interfering RNAs. J. Virol., 82, 5167-5177.
36. Wang, X.B., Jovel, J., Udomporn, P., Wang, Y., Wu, Q., Li, W.X., Gasciolli, V., Vaucheret, H., Ding, S.W. (2011) The 21-nucleotide, but not 22-nucleotide, viral secondary small interfering RNAs direct potent antiviral defense by two cooperative argonautes in Arabidopsis thaliana. Plant Cell, 23, 1625-1638.
37. Jaubert, M., Bhattacharjee, S., Mello, A.F.S., Perry, K.L., Moffett, P. (2011) ARGONAUTE2 mediates RNA-silencing antiviral defenses against potato virus X in Arabidopsis. Plant Physiol., 156, 1556-1564.
38. Harvey, J.J., Lewsey, M.G., Patel, K., Westwood, J., Heimstädt, S., Carr, J.P., Baulcombe, D.C. (2011) An antiviral defense role of AGO2 in plants. PLoS One, 6, e14639.
39. Qu, F., Ye, X., Morris, T.J. (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.
40. Ehsan, H., Reichheld, J.P., Durfee, T., Roe, J.L. (2004) TOUSLED kinase activity oscillates during the cell cycle and interacts with chromatin regulators. Plant Physiol., 134, 1488-1499.
41. Zeng, Y., Sankala, H., Zhang, X., Graves, P.R. (2008) Phosphorylation of Argonaute 2 at serine-387 facilitates its localization to processing bodies. Biochem. J., 413, 429-436.
42. Rüdel, S., Wang, Y., Lenobel, R., Körner, R., Hsiao, H.H., Urlaub, H., Patel, D., Meister, G. (2011) Phosphorylation of human Argonaute proteins affects small RNA binding. Nucleic Acids Res., 39, 2330-2343.
43. Fang, Y., Spector, D.L. (2007) Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr. Biol., 17, 818-823.
44. Wang, W., Ye, R., Xin, Y., Fang, X., Li, C., Shi, H., Zhou, X., Qi, Y. (2011) An importin- protein negatively regulates microRNA activity in Arabidopsis. Plant Cell, 23, 3565-3576.
45. Konstantin, I.I., Timofey, V.T., Tapio, I.H., Kristiina, M. (2005) The RISC component VIG is a target for dsRNA-independent protein kinase activity in Drosophila S2 cells. J. RNAi Gene Silenc., 1, 12-20.
46. Muddashetty, R.S., Nalavadi, V.C., Gross, C., Yao, X., Xing, L., Laur, O., Warren, S.T., Bassell, G.J. (2011) Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling. Mol. Cell, 42, 673-688.
47. Zhu, Y., Weng, M., Yang, Y., Zhang, C., Li, Z., Shen, W.H., Dong, A. (2011) Arabidopsis homologues of the histone chaperone ASF1 are crucial for chromatin replication and cell proliferation in plant development. Plant J., 66, 443-455.
48. Han, Z., Reifler, G.M., Saam, J.R., Mango, S.E., Schumacher, J.M. (2005) The Caenorhabditis elegans Tousled-like kinase contributes to chromosome segregation as a substrate and regulator of the Aurora B kinase. Curr. Biol., 15, 894-904.
49. Riefler, G.M., Dent, S.Y.R., Schumacher, J.M. (2008) Tousled-mediated activation of Aurora B kinase does not require Tousled kinase activity in vivo. J. Biol. Chem., 283, 12763-12768.
50. Adams, B.D., Claffey, K.P., White, B.A. (2009) Argonaute-2 expression is regulated by epidermal growth factor receptor and mitogen-activated protein kinase signaling and correlates with a transformed phenotype in breast cancer cells. Endocrinology, 150, 14-23.
51. Schott, G., Mari-Ordonez, A., Himber, C., Alioua, A., Voinnet, O., Dunoyer, P. (2012) Differential effects of viral silencing suppressors on siRNA and miRNA loading support the existence of two distinct cellular pools of ARGONAUTE1. EMBO J., 31, 2553-2565.
52. Meister, G. (2013) Argonaute proteins: functional insights and emerging roles. Nat. Rev. Genet., 25, 447-459.
53. Derrien, B., Baumberger, N., Schepetilnikov, M., Viotti, C., De Cillia, J., Ziegler-Graff, V., Isono, E., Schumacher, K., Genschik, P. (2012) Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. Proc. Natl. Acad. Sci. U.S.A., 109, 15942-15946.
54. Manavella, P.A., Hagmann, J., Ott, F., Laubinger, S., Franz, M., Macek, B., Weigel, D. (2012) Fast-forward genetics identifies plant CPL phosphatases as regulators of miRNA processing factor HYL1. Cell, 151, 859-870.