Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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Post-Translational Regulation of miRNA Pathway Components, AGO1 and HYL1, in Plants

  • Cho, Seok Keun (Department of Systems Biology, College of Life Science and Biotechnology, Yonsei University) ;
  • Ryu, Moon Young (Department of Systems Biology, College of Life Science and Biotechnology, Yonsei University) ;
  • Shah, Pratik (Department of Biomedical Engineering, University of California Irvine) ;
  • Poulsen, Christian Peter (Carlsberg Research Laboratory) ;
  • Yang, Seong Wook (Department of Systems Biology, College of Life Science and Biotechnology, Yonsei University)
  • Received : 2016.04.04
  • Accepted : 2016.06.10
  • Published : 2016.08.31
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Abstract

Post-translational modifications (PTMs) of proteins are essential to increase the functional diversity of the proteome. By adding chemical groups to proteins, or degrading entire proteins by phosphorylation, glycosylation, ubiquitination, neddylation, acetylation, lipidation, and proteolysis, the complexity of the proteome increases, and this then influences most biological processes. Although small RNAs are crucial regulatory elements for gene expression in most eukaryotes, PTMs of small RNA microprocessor and RNA silencing components have not been extensively investigated in plants. To date, several studies have shown that the proteolytic regulation of AGOs is important for host-pathogen interactions. DRB4 is regulated by the ubiquitin-proteasome system, and the degradation of HYL1 is modulated by a de-etiolation repressor, COP1, and an unknown cytoplasmic protease. Here, we discuss current findings on the PTMs of microprocessor and RNA silencing components in plants.

Keywords

References

  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. https://doi.org/10.1016/j.cub.2006.03.035
  2. Alvarado, V.Y., and Scholthof, H.B. (2011). AGO2, A new argonaute compromising plant virus accumulation. Front Plant Sci. 2, 112.
  3. Bartel, D.P. (2004). MicroRNAs, genomics, biogenesis, mechanism, and function. Cell 116, 281-297. https://doi.org/10.1016/S0092-8674(04)00045-5
  4. Baulcombe, D. (2004). RNA silencing in plants. Nature 431, 356-363. https://doi.org/10.1038/nature02874
  5. Baumberger, N., Tsai, C.H., Lie, M., Havecker, E., and Baulcombe, D.C. (2007). The Polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr. Biol. 17, 1609-1614. https://doi.org/10.1016/j.cub.2007.08.039
  6. Ben Chaabane, S., Liu, R., Chinnusamy, V., Kwon, Y., Park, J.H., Kim, S.Y., Zhu, J.K., Yang, S.W., and Lee, B.H. (2013). STA1, an Arabidopsis pre-mRNA processing factor 6 homolog, is a new player involved in miRNA biogenesis. Nucleic Acids Res. 41, 1984-1997. https://doi.org/10.1093/nar/gks1309
  7. Bielewicz, D., Kalak, M., Kalyna, M., Windels, D., Barta, A., Vazquez, F., Szweykowska-Kulinska, Z., and Jarmolowski, A. (2013). Introns of plant pri-miRNAs enhance miRNA biogenesis. EMBO Rep. 14, 622-628. https://doi.org/10.1038/embor.2013.62
  8. Bohmert, K., Camus, I., Bellini, C., Bouchez, D., Caboche, M., and Benning, C. (1998). AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J. 17, 170-180. https://doi.org/10.1093/emboj/17.1.170
  9. Bortolamiol, D., Pazhouhandeh, M., Marrocco, K., Genschik, P., and Ziegler-Graff, V. (2007). The Polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr. Biol. 17, 1615-1621. https://doi.org/10.1016/j.cub.2007.07.061
  10. Brodersen, P., and Voinnet, O. (2009). Revisiting the principles of microRNA target recognition and mode of action. Nat. Rev. Mol. Cell Biol. 10, 141-148.
  11. Callis, J. (2014). The ubiquitination machinery of the ubiquitin system. Arabidopsis Book 12, e0174. https://doi.org/10.1199/tab.0174
  12. Cardozo, T., and Pagano, M. (2004). The SCF ubiquitin ligase, insights into a molecular machine. Nat. Rev. Mol. Cell Biol. 5, 739-751.
  13. Chiu, M.H., Chen, I.H., Baulcombe, D.C., and Tsai, C.H. (2010). The silencing suppressor P25 of Potato virus X interacts with Argonaute1 and mediates its degradation through the proteasome pathway. Mol. Plant Pathol. 11, 641-649.
  14. Cho, S.K., Ben Chaabane, S., Shah, P., Poulsen, C.P., and Yang, S.W. (2014). COP1 E3 ligase protects HYL1 to retain microRNA biogenesis. Nat. Commun. 5, 5867. https://doi.org/10.1038/ncomms6867
  15. Curtin, S.J., Watson, J.M., Smith, N.A., Eamens, A.L., Blanchard, C.L., and Waterhouse, P.M. (2008). The roles of plant dsRNAbinding proteins in RNAi-like pathways. FEBS Lett. 582, 2753-2760. https://doi.org/10.1016/j.febslet.2008.07.004
  16. Denli, A.M., Tops, B.B., Plasterk, R.H., Ketting, R.F., and Hannon, G.J. (2004). Processing of primary microRNAs by the Microprocessor complex. Nature 432, 231-235. https://doi.org/10.1038/nature03049
  17. Derrien, B., Baumberger, N., Schepetilnikov, M., Viotti, C., De Cillia, J., Ziegler-Graff, V., Isono, E., Schumacher, K., and Genschik, P. (2012). Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. Proc. Natl. Acad. Sci. USA 109, 15942-15946. https://doi.org/10.1073/pnas.1209487109
  18. Dong, Z., Han, M.H., and Fedoroff, N. (2008). The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proc. Natl. Acad. Sci. USA 105, 9970-9975 https://doi.org/10.1073/pnas.0803356105
  19. Eamens, A.L., Wook Kim, K., and Waterhouse, P.M. (2012). DRB2, DRB3 and DRB5 function in a non-canonical microRNA pathway in Arabidopsis thaliana. Plant Signal. Behav. 7, 1224-1229. https://doi.org/10.4161/psb.21518
  20. Earley, K., Smith, M., Weber, R., Gregory, B., and Poethig, R. (2010). An endogenous F-box protein regulates ARGONAUTE1 in Arabidopsis thaliana. Silence 1, 15. https://doi.org/10.1186/1758-907X-1-15
  21. 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. https://doi.org/10.1261/rna.2455411
  22. Fusaro, A.F., Correa, R.L., Nakasugi, K., Jackson, C., Kawchuk, L., Vaslin, M.F., and Waterhouse, P.M. (2012). The Enamovirus P0 protein is a silencing suppressor which inhibits local and systemic RNA silencing through AGO1 degradation. Virology 426, 178-187. https://doi.org/10.1016/j.virol.2012.01.026
  23. Gasciolli, V., Mallory, A.C., Bartel, D.P., and 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. https://doi.org/10.1016/j.cub.2005.07.024
  24. Gu, S., Jin, L., Zhang, Y., Huang, Y., Zhang, F., Valdmanis, P.N., and Kay, M.A. (2012). The loop position of shRNAs and premiRNAs is critical for the accuracy of dicer processing in vivo. Cell 151, 900-911. https://doi.org/10.1016/j.cell.2012.09.042
  25. Hare, P.D., Seo, H.S., Yang, J.Y., and Chua, N.H. (2003). Modulation of sensitivity and selectivity in plant signaling by proteasomal destabilization. Curr. Opin. Plant Biol. 6, 453-462. https://doi.org/10.1016/S1369-5266(03)00080-3
  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/DRBfamily dsRNA-binding proteins in Arabidopsis thaliana. Plant Mol. Biol. 57, 173-188. https://doi.org/10.1007/s11103-004-6853-5
  27. Jakubiec, A., Yang, S.W., Chua, N.H. (2012). Arabidopsis DRB4 protein in antiviral defense against Turnip yellow mosaic virus infection. Plant J. 69, 14-25. https://doi.org/10.1111/j.1365-313X.2011.04765.x
  28. Kim, V.N. (2005). MicroRNA biogenesis, coordinated cropping and dicing. Nat. Rev. Mol. Cell Biol. 6, 376-385.
  29. Kraft, C., Peter, M., and Hofmann, K. (2010). Selective autophagy, ubiquitin-mediated recognition and beyond. Nat. Cell Biol. 12, 836-841. https://doi.org/10.1038/ncb0910-836
  30. Kurihara, Y., Takashi, Y., and Watanabe, Y. (2006). The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA 12, 206-212.
  31. Kwon, S.C., Nguyen, T.A., Choi, Y.G., Jo, M.H., Hohng, S., Kim, V.N., and Woo, J.S. (2016). Structure of human DROSHA. Cell 164, 81-90. https://doi.org/10.1016/j.cell.2015.12.019
  32. Landthaler, M., Yalcin, A., and Tuschl, T. (2004). The human DiGeorge syndrome critical region gene 8 and Its D. melanogaster homolog are required for miRNA biogenesis. Curr. Biol. 14, 2162-2167. https://doi.org/10.1016/j.cub.2004.11.001
  33. Lu, C., and Fedoroff, N. (2000). A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell 12, 2351-2366. https://doi.org/10.1105/tpc.12.12.2351
  34. Manavella, P.A., Hagmann, J., Ott, F., Laubinger, S., Franz, M., Macek, B., and Weigel, D. (2012). Fast-forward genetics identifies plant CPL phosphatases as regulators of miRNA processing factor HYL1. Cell 151, 859-870. https://doi.org/10.1016/j.cell.2012.09.039
  35. Meng, Y., Shao, C., Ma, X., and Wang, H. (2013). Introns targeted by plant microRNAs, a possible novel mechanism of gene regulation. Rice (N Y) 6, 8. https://doi.org/10.1186/1939-8433-6-8
  36. Moissiard, G., and 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. USA 103, 19593-19598. https://doi.org/10.1073/pnas.0604627103
  37. Myeku, N., and Figueiredo-Pereira, M.E. (2011). Dynamics of the degradation of ubiquitinated proteins by proteasomes and autophagy, association with sequestosome 1/p62. J. Biol. Chem. 286, 22426-22440. https://doi.org/10.1074/jbc.M110.149252
  38. 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. https://doi.org/10.1007/s11103-006-9125-8
  39. Nguyen, T.A., Jo, M.H., Choi, Y.G., Park, J., Kwon, S.C., Hohng, S., Kim, V.N., and Woo, J.S. (2015). Functional anatomy of the human microprocessor. Cell 161, 1374-1387 https://doi.org/10.1016/j.cell.2015.05.010
  40. Okamura, K., Hagen, J.W., Duan, H., Tyler, D.M., and Lai, E.C. (2007). The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 130, 89-100. https://doi.org/10.1016/j.cell.2007.06.028
  41. Parizotto, E.A., Dunoyer, P., Rahm, N., Himber, C., and Voinnet, O. (2004). In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes Dev. 18, 2237-2242. https://doi.org/10.1101/gad.307804
  42. Park, W., Li, J., Song, R., Messing, J., and Chen, X. (2002). CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol. 12, 1484-1495. https://doi.org/10.1016/S0960-9822(02)01017-5
  43. Pazhouhandeh, M., Dieterle, M., Marrocco, K., Lechner, E., Berry, B., Brault, V., Hemmer, O., Kretsch, T., Richards, K.E., Genschik, P., and Ziegler-Graff, V. (2006). F-box-like domain in the polerovirus protein P0 is required for silencing suppressor function. Proc. Natl. Acad. Sci. USA 103, 1994-1999. https://doi.org/10.1073/pnas.0510784103
  44. Pfeffer, S., Dunoyer, P., Heim, F., Richards, K.E., Jonard, G., and Ziegler-Graff, V. (2002). P0 of beet Western yellows virus is a suppressor of posttranscriptional gene silencing. J. Virol. 76, 6815-6824. https://doi.org/10.1128/JVI.76.13.6815-6824.2002
  45. Raja, P., Jackel, J.N., Li, S., Heard, I.M., and Bisaro, D.M. (2014). Arabidopsis double-stranded RNA binding protein DRB3 participates in methylation-mediated defense against geminiviruses. J. Virol. 88, 2611-2622. https://doi.org/10.1128/JVI.02305-13
  46. Ren, G., and Yu, B. (2012). Critical roles of RNA-binding proteins in miRNA biogenesis in Arabidopsis. RNA Biol. 9, 1424-1428. https://doi.org/10.4161/rna.22740
  47. Rock, K.L., and Goldberg, A.L. (1999). Degradation of cell proteins and the generation of MHC class I-presented peptides. Annu. Rev. Immunol. 17, 739-779. https://doi.org/10.1146/annurev.immunol.17.1.739
  48. Rogers K, and Chen X (2013). Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25, 2383-2399. https://doi.org/10.1105/tpc.113.113159
  49. Saito, K., Ishizuka, A., Siomi, H., and Siomi, M.C. (2005). Processing of pre-microRNAs by the Dicer-1-Loquacious complex in Drosophila cells. PLoS Biol. 3, e235. https://doi.org/10.1371/journal.pbio.0030235
  50. Shah, P., Rorvig-Lund, A., Chaabane, S.B., Thulstrup, P.W., Kjaergaard, H.G., Fron, E., Hofkens, J., Yang, S.W., and Vosch,T. (2012). Design aspects of bright red emissive silver nanoclusters/ DNA probes for microRNA detection. ACS Nano 6, 8803-8814. https://doi.org/10.1021/nn302633q
  51. Shah, P., Thulstrup, P.W., Cho, S.K., Bjerrum, M.J., and Yang, S.W. (2014) DNA-RNA chimera indicates the flexibility of the backbone influences the encapsulation of fluorescent AgNC emitters. Chem. Commun. 50, 13592-13595. https://doi.org/10.1039/C4CC06439A
  52. Shah, P., Choi, S.W., Kim, H.J., Cho, S.K., Thulstrup, P.W., Bjerrum, M.J., Bhang, Y.J., Ahn, J.C., and Yang, S.W. (2015). DNA/RNA chimera templates improve the emission intensity and target the accessibility of silver nanocluster-based sensors for human microRNA detection. Analyst 140, 3422-3430. https://doi.org/10.1039/C5AN00093A
  53. Speth, C., Willing, E.M., Rausch, S., Schneeberger, K., and Laubinger, S. (2013). RACK1 scaffold proteins influence miRNA abundance in Arabidopsis. Plant J. 76, 433-445. https://doi.org/10.1111/tpj.12308
  54. Valencia-Sanchez, M.A., Liu, J., Hannon, G.J., and Parker, R. (2006). Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 20, 515-524. https://doi.org/10.1101/gad.1399806
  55. Vaucheret, H., Vazquez, F., Crete, P., and Bartel, D.P. (2004). The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev. 18, 1187-1197. https://doi.org/10.1101/gad.1201404
  56. Vaucheret, H., Mallory, A.C., and Bartel, D.P. (2006) AGO1 homeostasis entails coexpression of MIR168 and AGO1 and preferential stabilization of miR168 by AGO1. Mol. Cell 22, 129-136. https://doi.org/10.1016/j.molcel.2006.03.011
  57. Voinnet, O. (2005). Induction and suppression of RNA silencing, insights from viral infections. Nat. Rev. Genet. 6, 206-220. https://doi.org/10.1038/nrg1555
  58. Voinnet, O. (2009). Origin, biogenesis, and activity of plant microRNAs. Cell 136, 669-687. https://doi.org/10.1016/j.cell.2009.01.046
  59. von Arnim, A.G. (2001). A hitchhiker's guide to the proteasome. Sci STKE 2001, pe2.
  60. Wu, X., Shi, Y., Li, J., Xu, L., Fang, Y., Li, X., and Qi, Y. (2013). A role for the RNA-binding protein MOS2 in microRNA maturation in Arabidopsis. Cell Res. 23, 645-657. https://doi.org/10.1038/cr.2013.23
  61. 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. https://doi.org/10.1371/journal.pbio.0020104
  62. Yang, S.W., and Vosch, T. (2011). Rapid detection of microRNA by a silver nanocluster DNA probe. Anal Chem 83, 6935-6939. https://doi.org/10.1021/ac201903n
  63. Yang, S.W., Chen, H.Y., Yang, J., Machida, S., Chua, N.H., and Yuan, Y.A. (2010). Structure of Arabidopsis HYPONASTIC LEAVES1 and its molecular implications for miRNA processing. Structure 18, 594-605. https://doi.org/10.1016/j.str.2010.02.006
  64. Zeng, Y., Yi, R., and Cullen, B.R. (2005). Recognition and cleavage of primary microRNA precursors by the nuclear processing enzyme Drosha. EMBO J. 24, 138-148. https://doi.org/10.1038/sj.emboj.7600491
  65. Zhan, X., Wang, B., Li, H., Liu, R., Kalia, R.K., Zhu, J.K., and Chinnusamy, V. (2012). Arabidopsis proline-rich protein important for development and abiotic stress tolerance is involved in microRNA biogenesis. Proc. Natl. Acad. Sci. USA 109, 18198-18203 https://doi.org/10.1073/pnas.1216199109
  66. Zhang, X., Yuan, Y.R., Pei, Y., Lin, S.S., Tuschl, T., Patel, D.J., and Chua, N.H. (2006). Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev. 20, 3255-3268. https://doi.org/10.1101/gad.1495506
  67. Zhang, S., Xie, M., Ren, G., and Yu, B. (2013). CDC5, a DNA binding protein, positively regulates posttranscriptional processing and/or transcription of primary microRNA transcripts. Proc. Natl. Acad. Sci. USA 110, 17588-17593. https://doi.org/10.1073/pnas.1310644110
  68. Zhang, S., Liu, Y., and Yu, B. (2014). PRL1, an RNA-binding protein, positively regulates the accumulation of miRNAs and siRNAs in Arabidopsis. PLoS Genet. 10, e1004841. https://doi.org/10.1371/journal.pgen.1004841

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