Biogenesis of trans-acting siRNAs, endogenoussecondary siRNAs in plants

Genes and Genetic Systems

Volumn 88, Issue 2, 2013, Pages 77-84

  Yoshikawa, Manabu ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

ARGONAUTE; DICER LIKE; microRNA; RNA induced silencing complex; trans acting siRNA

Indexed keywords

ARGONAUTE 1 PROTEIN; ARGONAUTE 2 PROTEIN; ARGONAUTE 5 PROTEIN; ARGONAUTE PROTEIN; DICER; DICER LIKE 4; DOUBLE STRANDED RNA; EXPORTIN 5; HASTY PROTEIN; MICRORNA; MICRORNA 390; PLANT RNA; RNA DIRECTED RNA POLYMERASE; RNA DIRECTED RNA POLYMERASE 6; SMALL INTERFERING RNA; TRANS ACTING SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARABIDOPSIS THALIANA; BIOGENESIS; CELL NUCLEUS; CELLULAR DISTRIBUTION; CYTOPLASM; CYTOSOL; GENETIC SCREENING; LOSS OF FUNCTION MUTATION; NONHUMAN; POSTTRANSCRIPTIONAL GENE SILENCING; PROTEIN LOCALIZATION; REVIEW; RIBOSOME; RNA CLEAVAGE; RNA PROCESSING;

BIOGENESIS; GENE EXPRESSION REGULATION, PLANT; PLANTS; RNA, PLANT; RNA, SMALL INTERFERING;

EID: 84879997345     PISSN: 13417568     EISSN: 18805779     Source Type: Journal    
DOI: 10.1266/ggs.88.77     Document Type: Review

References (69)

1. Adenot, X., Elmayan, T., Lauressergues, D., Boutet, S., Bouche, N., Gasciolli, V., and Vaucheret, H. (2006) DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr. Biol. 16, 927-932.
2. Allen, E., and Howell, M. D. (2010) MiRNAs in the biogenesis of trans-acting siRNAs in higher plants. Semin. Cell Dev. Biol. 21, 798-804.
3. Allen, E., Xie, Z., Gustafson, A. M., and Carrington, J. C. (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121, 207-221.
4. Axtell, M. J. (2013) Classification and Comparison of Small RNAs from Plants. Annu. Rev. Plant Biol. 64, 137-159.
5. Axtell, M. J., Jan, C., Rajagopalan, R., and Bartel, D. P. (2006) A two-hit trigger for siRNA biogenesis in plants. Cell 127, 565-577.
6. Baulcombe, D. C. (2007) Amplified silencing. Science 315, 199-200.
7. Baumberger, N., and Baulcombe, D. C. (2005) ArabidopsisARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl. Acad. Sci. USA 102, 11928-11933.
8. Borges, F., Pereira, P. A., Slotkin, R. K., Martienssen, R. A., and Becker, J. D. (2011) MicroRNA activity in the Arabidopsismale germline. J. Exp. Bot. 62, 1611-1620.
9. Borsani, O., Zhu, J., Verslues, P. E., Sunkar, R., and Zhu, J. K.(2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123, 1279-1291.
10. Bouche, N., Lauressergues, D., Gasciolli, V., and 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.
11. Carbonell, A., Fahlgren, N., Garcia-Ruiz, H., Gilbert, K. B., Montgomery, T. A., Nguyen, T., Cuperus, J. T., and Carrington, J. C. (2012) Functional analysis of three Arabidopsis ARGONAUTES using slicer-defective mutants. Plant Cell 24, 3613-3629.
12. Chen, H. M., Chen, L. T., Patel, K., Li, Y. H., Baulcombe, D. C., and Wu, S. H. (2010) 22-nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proc. Natl. Acad. Sci. USA 107, 15269-15274.
13. Cuperus, J. T., Carbonell, A., Fahlgren, N., Garcia-Ruiz, H., Burke, R. T., Takeda, A., Sullivan, C. M., Gilbert, S. D., Montgomery, T. A., and Carrington, J. C. (2010) Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat. Struct. Mol. Biol. 17, 997-1003.
14. Curaba, J., and Chen, X. (2008) Biochemical activities of Arabidopsis RNA-dependent RNA polymerase 6. J. Biol. Chem. 283, 3059-3066.
15. Ding, S. W. (2010) RNA-based antiviral immunity. Nat. Rev. Immunol. 10, 632-644.
16. Earley, K. W., and Poethig, R. S. (2011) Binding of the cyclophilin 40 ortholog SQUINT to Hsp90 protein is required for SQUINT function in Arabidopsis. J. Biol. Chem. 286, 38184-38189.
17. Fahlgren, N., Montgomery, T. A., Howell, M. D., Allen, E., Dvorak, S. K., Alexander, A. L., and Carrington, J. C. (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr. Biol. 16, 939-944.
18. Felippes, F. F., and Weigel, D. (2009) Triggering the formation of tasiRNAs in Arabidopsis thaliana: the role of microRNA miR173. EMBO Rep. 10, 264-270.
19. Finnegan, E. J., Margis, R., and Waterhouse, P. M. (2003) Posttranscriptional gene silencing is not compromised in the Arabidopsis CARPEL FACTORY (DICER-LIKE1) mutant, a homolog of Dicer-1 from Drosophila. Curr. Biol. 13, 236-240.
20. Fukudome, A., Kanaya, A., Egami, M., Nakazawa, Y., Hiraguri, A., Moriyama, H., and Fukuhara, T. (2011) Specific requirement of DRB4, a dsRNA-binding protein, for the in vitro dsRNA-cleaving activity of Arabidopsis Dicer-like 4. RNA 17, 750-760.
21. Fukunaga, R., and Doudna, J. A. (2009) DsRNA with 5′ overhangs contributes to endogenous and antiviral RNA silencing pathways in plants. EMBO J. 28, 545-555.
22. Garcia, D., Collier, S. A., Byrne, M. E., and Martienssen, R. A.(2006) Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr. Biol. 16, 933-938.
23. Hannon, G. J. (2002) RNA interference. Nature 418, 244-251.
24. Henderson, I. R., Zhang, X., Lu, C., Johnson, L., Meyers, B. C., Green, P. J., and Jacobsen, S. E. (2006) Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nat. Genet. 38, 721-725.
25. Hernandez-Pinzon, I., Yelina, N. E., Schwach, F., Studholme, D. J., Baulcombe, D. C., and Dalmay, T. (2007) SDE5, the putative homologue of a human mRNA export factor, is required for transgene silencing and accumulation of trans-acting endogenous siRNA. Plant J. 50, 140-148.
26. Hiraguri, A., Itoh, R., Kondo, N., Nomura, Y., Aizawa, D., Murai, Y., Koiwa, H., Seki, M., Shinozaki, K., and Fukuhara, T.(2005) Specific interactions between Dicer-like proteins and HYL1/DRB-family dsRNA-binding proteins in Arabidopsis thaliana. Plant Mol. Biol. 57, 173-188.
27. Hoffer, P., Ivashuta, S., Pontes, O., Vitins, A., Pikaard, C., Mroczka, A., Wagner, N., and Voelker, T. (2011) Posttranscriptional gene silencing in nuclei. Proc. Natl. Acad. Sci. USA 108, 409-414.
28. Howell, M. D., Fahlgren, N., Chapman, E. J., Cumbie, J. S., Sullivan, C. M., Givan, S. A., Kasschau, K. D., and Carrington, J. C. (2007) Genome-wide analysis of the RNA-DEPENDENT RNA POLYMERASE6/DICER-LIKE4 pathway in Arabidopsis reveals dependency on miRNA-and tasiRNA-directed targeting. Plant Cell 19, 926-942.
29. Hunter, C., Willmann, M. R., Wu, G., Yoshikawa, M., de la Luz Gutierrez-Nava, M., and Poethig, R. S. (2006) Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 133, 2973-2981.
30. Iki, T., Yoshikawa, M., Nishikiori, M., Jaudal, M. C., Matsumoto-Yokoyama, E., Mitsuhara, I., Meshi, T., and Ishikawa, M.(2010) In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaperone HSP90. Mol. Cell 39, 282-291.
31. Iki, T., Yoshikawa, M., Meshi, T., and Ishikawa, M. (2012) Cyclophilin 40 facilitates HSP90-mediated RISC assembly in plants. EMBO J. 31, 267-278.
32. Jauvion, V., Elmayan, T., and Vaucheret, H. (2010) The conserved RNA trafficking proteins HPR1 and TEX1 are involved in the production of endogenous and exogenous small interfering RNA in Arabidopsis. Plant Cell 22, 2697-2709.
33. Jouannet, V., Moreno, A. B., Elmayan, T., Vaucheret, H., Crespi, M. D., and Maizel, A. (2012) Cytoplasmic Arabidopsis AGO7 accumulates in membrane-associated siRNA bodies and is required for ta-siRNA biogenesis. EMBO J. 31, 1704-1713.
34. Kanno, T., Yoshikawa, M., and Habu, Y. (2013) Locus-specific requirements of DDR complexes for gene-body methylation of TAS genes in Arabidopsis thaliana. Plant Mol. Biol. Rep. in press.
35. Katiyar-Agarwal, S., Morgan, R., Dahlbeck, D., Borsani, O., Villegas, A., Jr., Zhu, J. K., Staskawicz, B. J., and Jin, H.(2006) A pathogen-inducible endogenous siRNA in plant immunity. Proc. Natl. Acad. Sci. USA 103, 18002-18007.
36. Kawamata, T., Seitz, H., and Tomari, Y. (2009) Structural determinants of miRNAs for RISC loading and slicer-independent unwinding. Nat. Struct. Mol. Biol. 16, 953-960.
37. Kumakura, N., Takeda, A., Fujioka, Y., Motose, H., Takano, R., and Watanabe, Y. (2009) SGS3 and RDR6 interact and colocalize in cytoplasmic SGS3/RDR6-bodies. FEBS Lett. 583, 1261-1266.
38. Kurihara, Y., and Watanabe, Y. (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc. Natl. Acad. Sci. USA 101, 12753-12758.
39. Mi, S., Cai, T., Hu, Y., Chen, Y., Hodges, E., Ni, F., Wu, L., Li, S., Zhou, H., Long, C., et al. (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′terminal nucleotide. Cell 133, 116-127.
40. Mlotshwa, S., Pruss, G. J., Peragine, A., Endres, M. W., Li, J., Chen, X., Poethig, R. S., Bowman, L. H., and Vance, V.(2008) DICER-LIKE2 plays a primary role in transitive silencing of transgenes in Arabidopsis. PLoS One 3, e1755.
41. Montgomery, T. A., Howell, M. D., Cuperus, J. T., Li, D., Hansen, J. E., Alexander, A. L., Chapman, E. J., Fahlgren, N., Allen, E., and Carrington, J. C. (2008a) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133, 128-141.
42. Montgomery, T. A., Yoo, S. J., Fahlgren, N., Gilbert, S. D., Howell, M. D., Sullivan, C. M., Alexander, A., Nguyen, G., Allen, E., Ahn, J. H., et al. (2008b) AGO1-miR173 complex initiates phased siRNA formation in plants. Proc. Natl. Acad. Sci. USA 105, 20055-20062.
43. Mukherjee, K., Campos, H., and Kolaczkowski, B. (2013) Evolution of animal and plant dicers: early parallel duplications and recurrent adaptation of antiviral RNA binding in plants. Mol. Biol. Evol. 30, 627-641.
44. Nakazawa, Y., Hiraguri, A., Moriyama, H., and Fukuhara, T.(2007) The dsRNA-binding 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.
45. Nonomura, K., Morohoshi, A., Nakano, M., Eiguchi, M., Miyao, A., Hirochika, H., and Kurata, N. (2007) A germ cell-specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. Plant Cell 19, 2583-2594.
46. Park, M. Y., Wu, G., Gonzalez-Sulser, A., Vaucheret, H., and Poethig, R. S. (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc. Natl. Acad. Sci. USA 102, 3691-3696.
47. Peragine, A., Yoshikawa, M., Wu, G., Albrecht, H. L., and Poethig, R. S. (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev. 18, 2368-2379.
48. Qi, Y., He, X., Wang, X. J., Kohany, O., Jurka, J., and Hannon, G. J. (2006) Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443, 1008-1012.
49. Qian, Y., Cheng, Y., Cheng, X., Jiang, H., Zhu, S., and Cheng, B.(2011) Identification and characterization of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families in maize. Plant Cell Rep. 30, 1347-1363.
50. Rajagopalan, R., Vaucheret, H., Trejo, J., and Bartel, D. P.(2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 20, 3407-3425.
51. Sijen, T., Fleenor, J., Simmer, F., Thijssen, K. L., Parrish, S., Timmons, L., Plasterk, R. H., and Fire, A. (2001) On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107, 465-476.
52. Singh, M., Goel, S., Meeley, R. B., Dantec, C., Parrinello, H., Michaud, C., Leblanc, O., and Grimanelli, D. (2011) Production of viable gametes without meiosis in maize deficient for an ARGONAUTE protein. Plant Cell 23, 443-458.
53. Song, X., Li, P., Zhai, J., Zhou, M., Ma, L., Liu, B., Jeong, D. H., Nakano, M., Cao, S., Liu, C., et al. (2012) Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J. 69, 462-474.
54. Souret, F. F., Kastenmayer, J. P., and Green, P. J. (2004) AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol. Cell 15, 173-183.
55. Takeda, A., Iwasaki, S., Watanabe, T., Utsumi, M., and Watanabe, Y. (2008) The mechanism selecting the guide strand from small RNA duplexes is different among Argonaute proteins. Plant Cell Physiol. 49, 493-500.
56. Vaistij, F. E., Jones, L., and Baulcombe, D. C. (2002) Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA-dependent RNA polymerase. Plant Cell 14, 857-867.
57. Vaucheret, H. (2008) Plant ARGONAUTES. Trends Plant Sci. 13, 350-358.
58. Vazquez, F., Vaucheret, H., Rajagopalan, R., Lepers, C., Gasciolli, V., Mallory, A. C., Hilbert, J. L., Bartel, D. P., and Crete, P.(2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol. Cell 16, 69-79.
59. Voinnet, O. (2008) Use, tolerance and avoidance of amplified RNA silencing by plants. Trends Plant Sci. 13, 317-328.
60. Wang, W., Ye, R., Xin, Y., Fang, X., Li, C., Shi, H., Zhou, X., and Qi, Y. (2011) An importin beta protein negatively regulates microRNA activity in Arabidopsis. Plant Cell 23, 3565-3576.
61. Wu, L., Zhang, Q., Zhou, H., Ni, F., Wu, X., and Qi, Y. (2009) Rice microRNA effector complexes and targets. Plant Cell 21, 3421-3435.
62. Wu, L., Mao, L., and Qi, Y. (2012) Roles of DICER-LIKE and ARGONAUTE proteins in TAS-derived small interfering RNA-triggered DNA methylation. Plant Physiol. 160, 990-999.
63. Xie, Z., Kasschau, K. D., and Carrington, J. C. (2003) Negative feedback regulation of Dicer-Like1 in Arabidopsis by microRNA-guided mRNA degradation. Curr. Biol. 13, 784-789.
64. Xie, Z., Johansen, L. K., Gustafson, A. M., Kasschau, K. D., Lellis, A. D., Zilberman, D., Jacobsen, S. E., and Carrington, J. C.(2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, E104.
65. Xie, Z., Allen, E., Wilken, A., and Carrington, J. C. (2005) DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 102, 12984-12989.
66. Yelina, N. E., Smith, L. M., Jones, A. M., Patel, K., Kelly, K. A., and Baulcombe, D. C. (2010) Putative Arabidopsis THO/TREX mRNA export complex is involved in transgene and endogenous siRNA biosynthesis. Proc. Natl. Acad. Sci. USA 107, 13948-13953.
67. Yoshikawa, M., Peragine, A., Park, M. Y., and Poethig, R. S.(2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev. 19, 2164-2175.
68. Yoshikawa, M., Iki, T., Tsutsui, Y., Miyashita, K., Poethig, R. S., Habu, Y., and Ishikawa, M. (2013) 3′ fragment of miR173-programmed RISC-cleaved RNA is protected from degradation in a complex with RISC and SGS3. Proc. Natl. Acad. Sci. USA 110, 4117-4122.
69. Zhang, C., Ng, D. W., Lu, J., and Chen, Z. J. (2012) Roles of target site location and sequence complementarity in trans-acting siRNA formation in Arabidopsis. Plant J. 69, 217-226.