Nucleotide bias of DCL and AGO in plant anti-virus gene silencing

Abstract

Plant Dicer-like (DCL) and Argonaute (AGO) are the key enzymes involved in anti-virus post-transcriptional gene silencing (AV-PTGS). Here we show that AV-PTGS exhibited nucleotide preference by calculating a relative AV-PTGS efficiency on processing viral RNA substrates. In comparison with genome sequences of dicot-infecting Turnip mosaic virus (TuMV) and monocot-infecting Cocksfoot streak virus (CSV), viral-derived small interfering RNAs (vsiRNAs) displayed positive correlations between AV-PTGS efficiency and G+C content (GC%). Further investigations on nucleotide contents revealed that the vsiRNA populations had G-biases. This finding was further supported by our analyses of previously reported vsiRNA populations in diverse plant-virus associations, and AGO associated Arabidopsis endogenous siRNA populations, indicating that plant AGOs operated with G-preference. We further propose a hypothesis that AV-PTGS imposes selection pressure(s) on the evolution of plant viruses. This hypothesis was supported when potyvirus genomes were analysed for evidence of GC elimination, suggesting that plant virus evolution to have low GC% genomes would have a unique function, which is to reduce the host AV-PTGS attack during infections.

Keywords

anti-virus post-transcriptional gene silencing / siRNA / nucleotide bias / Dicer-like / Argonaute / plant virus evolution

References

[1] Aliyari, R., and Ding, S.W. (2009). RNA-based viral immunity initiated by the Dicer family of host immune receptors. Immunol Rev 227, 176–188 .10.1111/j.1600-065X.2008.00722.x
[2] Brackney, D.E., Beane, J.E., Ebel, G.D., and Holmes, E.C. (2009). RNAi targeting of West Nile virus in mosquito midguts promotes virus diversification. PLoS Pathog 5, e1000502.10.1371/journal.ppat.1000502
[3] Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y.Y., Sieburth, L., and Voinnet, O. (2008). Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185–1190 .10.1126/science.1159151
[4] Burgyán, J. (2008). Role of silencing suppressor proteins. Methods Mol Biol 451, 69–79 .10.1007/978-1-59745-102-4_5
[5] Chan, S.W., Henderson, I.R., and Jacobsen, S.E. (2005). Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6, 351–360 .10.1038/nrg1601
[6] Crooks, G.E., Hon, G., Chandonia, J.M., and Brenner, S.E. (2004). WebLogo: a sequence logo generator. Genome Res 14, 1188–1190 .10.1101/gr.849004
[7] Czech, B., Malone, C.D., Zhou, R., Stark, A., Schlingeheyde, C., Dus, M., Perrimon, N., Kellis, M., Wohlschlegel, J.A., Sachidanandam, R., . (2008). An endogenous small interfering RNA pathway in Drosophila. Nature 453, 798–802 .10.1038/nature07007
[8] Deleris, A., Gallego-Bartolome, J., Bao, J., Kasschau, K.D., Carrington, J.C., and Voinnet, O. (2006). Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313, 68–71 .10.1126/science.1128214
[9] Ding, S.W., and Voinnet, O. (2007). Antiviral immunity directed by small RNAs. Cell 130, 413–426 .
[10] Donaire, L., Barajas, D., Martínez-García, B., Martínez-Priego, L., Pagán, I., and Llave, C. (2008). Structural and genetic requirements for the biogenesis of tobacco rattle virus-derived small interfering RNAs. J Virol 82, 5167–5177 .10.1128/JVI.00272-08
[11] Donaire, L., Wang, Y., Gonzalez-Ibeas, D., Mayer, K.F., Aranda, M.A., and Llave, C. (2009). Deep-sequencing of plant viral small RNAs reveals effective and widespread targeting of viral genomes. Virology 392, 203–214 .10.1016/j.virol.2009.07.005
[12] Du, Q.S., Duan, C.G., Zhang, Z.H., Fang, Y.Y., Fang, R.X., Xie, Q., and Guo, H.S. (2007). DCL4 targets Cucumber mosaic virus satellite RNA at novel secondary structures. J Virol 81, 9142–9151 .10.1128/JVI.02885-06
[13] Elena, S.F., Agudelo-Romero, P., Carrasco, P., Codo?er, F.M., Martín, S., Torres-Barceló, C., and Sanjuán, R. (2008). Experimental evolution of plant RNA viruses. Heredity 100, 478–483 .10.1038/sj.hdy.6801088
[14] Fahlgren, N., Howell, M.D., Kasschau, K.D., Chapman, E.J., Sullivan, C.M., Cumbie, J.S., Givan, S.A., Law, T.F., Grant, S.R., Dangl, J.L., . (2007). High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE 2, e219.10.1371/journal.pone.0000219
[15] Grimm, D., and Kay, M.A. (2007). Combinatorial RNAi: a winning strategy for the race against evolving targets?Mol Ther 15, 878–888 .
[16] Havecker, E.R., Wallbridge, L.M., Hardcastle, T.J., Bush, M.S., Kelly, K.A., Dunn, R.M., Schwach, F., Doonan, J.H., and Baulcombe, D.C. (2010). The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 22, 321–334 .10.1105/tpc.109.072199
[17] Hershberg, R., and Petrov, D.A. (2008). Selection on codon bias. Annu Rev Genet 42, 287–299 .10.1146/annurev.genet.42.110807.091442
[18] Ho, T., Pallett, D., Rusholme, R., Dalmay, T., and Wang, H. (2006). A simplified method for cloning of short interfering RNAs from Brassica juncea infected with Turnip mosaic potyvirus and Turnip crinkle carmovirus. J Virol Methods 136, 217–223 .10.1016/j.jviromet.2006.05.016
[19] Ho, T., Wang, H., Pallett, D., and Dalmay, T. (2007). Evidence for targeting common siRNA hotspots and GC preference by plant Dicer-like proteins. FEBS Lett 581, 3267–3272 .10.1016/j.febslet.2007.06.022
[20] Ho, T., Rusholme Pilcher, R.L., Edwards, M.L., Cooper, I., Dalmay, T., and Wang, H. (2008). Evidence for GC preference by monocot Dicer-like proteins. Biochem Biophys Res Commun 368, 433–437 .10.1016/j.bbrc.2008.01.110
[21] H?ck, J., and Meister, G. (2008). The Argonaute protein family. Genome Biol 9, 210.10.1186/gb-2008-9-2-210
[22] Hutvagner, G., and Simard, M.J. (2008). Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 9, 22–32 .10.1038/nrm2321
[23] Jinek, M., and Doudna, J.A. (2009). A three-dimensional view of the molecular machinery of RNA interference. Nature 457, 405–412 .10.1038/nature07755
[24] Kasschau, K.D., Fahlgren, N., Chapman, E.J., Sullivan, C.M., Cumbie, J.S., Givan, S.A., and Carrington, J.C. (2007). Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol 5, e57.10.1371/journal.pbio.0050057
[25] Linsen, S.E., de Wit, E., Janssens, G., Heater, S., Chapman, L., Parkin, R.K., Fritz, B., Wyman, S.K., de Bruijn, E., Voest, E.E., . (2009). Limitations and possibilities of small RNA digital gene expression profiling. Nat Methods 6, 474–476 .10.1038/nmeth0709-474
[26] Lister, R., O’Malley, R.C., Tonti-Filippini, J., Gregory, B.D., Berry, C.C., Millar, A.H., and Ecker, J.R. (2008). Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133, 523–536 .
[27] Liu, B., Chen, Z., Song, X., Liu, C., Cui, X., Zhao, X., Fang, J., Xu, W., Zhang, H., Wang, X., . (2007). Oryza sativa dicer-like4 reveals a key role for small interfering RNA silencing in plant development. Plant Cell 19, 2705–2718 .10.1105/tpc.107.052209
[28] Ma, J.B., Yuan, Y.R., Meister, G., Pei, Y., Tuschl, T., and Patel, D.J. (2005). Structural basis for 5'-end-specific recognition of guide RNA by the A. fulgidus Piwi protein. Nature 434, 666–670 .10.1038/nature03514
[29] Matranga, C., Tomari, Y., Shin, C., Bartel, D.P., and Zamore, P.D. (2005). Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 123, 607–620 .
[30] Matzke, M., Kanno, T., Huettel, B., Daxinger, L., and Matzke, A.J. (2007). Targets of RNA-directed DNA methylation. Curr Opin Plant Biol 10, 512–519 .10.1016/j.pbi.2007.06.007
[31] Mi, S., Cai, T., Hu, Y., Chen, Y., Hodges, E., Ni, F., Wu, L., Li, S., Zhou, H., Long, C., . (2008). Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133, 116–127 .
[32] Mlotshwa, S., Pruss, G.J., and Vance, V. (2008). Small RNAs in viral infection and host defense. Trends Plant Sci 13, 375–382 .10.1016/j.tplants.2008.04.009
[33] Molnár, A., Csorba, T., Lakatos, L., Várallyay, E., Lacomme, C., and Burgyán, J. (2005). Plant virus-derived small interfering RNAs originate predominantly from highly structured single-stranded viral RNAs. J Virol 79, 7812–7818 .10.1128/JVI.79.12.7812-7818.2005
[34] 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. (2008). Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133, 128–141 .
[35] Navarro, B., Pantaleo, V., Gisel, A., Moxon, S., Dalmay, T., Bisztray, G., Di Serio, F., Burgyán, J., and Liu, D.X. (2009). Deep sequencing of viroid-derived small RNAs from grapevine provides new insights on the role of RNA silencing in plant-viroid interaction. PLoS ONE 4, e7686.10.1371/journal.pone.0007686
[36] Ohshima, K., Akaishi, S., Kajiyama, H., Koga, R., and Gibbs, A.J. (2010). Evolutionary trajectory of turnip mosaic virus populations adapting to a new host. J Gen Virol 91, 788–801 .10.1099/vir.0.016055-0
[37] Parker, J.S., Roe, S.M., and Barford, D. (2005). Structural insights into mRNA recognition from a PIWI domain-siRNA guide complex. Nature 434, 663–666 .10.1038/nature03462
[38] Pei, Y., and Tuschl, T. (2006). On the art of identifying effective and specific siRNAs. Nat Methods 3, 670–676 .10.1038/nmeth911
[39] Qi, X., Bao, F.S., Xie, Z., and Aramayo, R. (2009). Small RNA deep sequencing reveals role for Arabidopsis thaliana RNA-dependent RNA polymerases in viral siRNA biogenesis. PLoS ONE 4, e4971.10.1371/journal.pone.0004971
[40] 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 .10.1101/gad.1476406
[41] Rashid, U.J., Paterok, D., Koglin, A., Gohlke, H., Piehler, J., and Chen, J.C. (2007). Structure of Aquifex aeolicus argonaute highlights conformational flexibility of the PAZ domain as a potential regulator of RNA-induced silencing complex function. J Biol Chem 282, 13824–13832 .10.1074/jbc.M608619200
[42] Ruiz-Ferrer, V., and Voinnet, O. (2009). Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60, 485–510 .10.1146/annurev.arplant.043008.092111
[43] 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 .10.1093/pcp/pcn043
[44] Tan, Z., Gibbs, A.J., Tomitaka, Y., Sánchez, F., Ponz, F., and Ohshima, K. (2005). Mutations in Turnip mosaic virus genomes that have adapted to Raphanus sativus. J Gen Virol 86, 501–510 .10.1099/vir.0.80540-0
[45] Tomari, Y., Du, T., Haley, B., Schwarz, D.S., Bennett, R., Cook, H.A., Koppetsch, B.S., Theurkauf, W.E., and Zamore, P.D. (2004). RISC assembly defects in the Drosophila RNAi mutant armitage. Cell 116, 831–841 .
[46] Vaucheret, H. (2008). Plant ARGONAUTES. Trends Plant Sci 13, 350–358 .10.1016/j.tplants.2008.04.007
[47] Vetsigian, K., and Goldenfeld, N. (2009). Genome rhetoric and the emergence of compositional bias. Proc Natl Acad Sci U S A 106, 215–220 .10.1073/pnas.0810122106
[48] Wang, H., Huang, L.F., and Cooper, J.I. (2006). Analyses on mutation patterns, detection of population bottlenecks, and suggestion of deleterious-compensatory evolution among members of the genus Potyvirus. Arch Virol 151, 1625–1633 .
[49] Watanabe, T., Umehara, T., and Kohara, M. (2007). Therapeutic application of RNA interference for hepatitis C virus. Adv Drug Deliv Rev 59, 1263–1276 .10.1016/j.addr.2007.03.022
[50] Wei, Y., Chen, S., Yang, P., Ma, Z., and Kang, L. (2009). Characterization and comparative profiling of the small RNA transcriptomes in two phases of locust. Genome Biol 10, R6.10.1186/gb-2009-10-1-r6
[51] Yamamoto, T., and Tsunetsugu-Yokota, Y. (2008). Prospects for the therapeutic application of lentivirus-based gene therapy to HIV-1 infection. Curr Gene Ther 8, 1–8 .10.2174/156652308783688536
[52] Yang, Z., and Nielsen, R. (2008). Mutation-selection models of codon substitution and their use to estimate selective strengths on codon usage. Mol Biol Evol 25, 568–579 .10.1093/molbev/msm284
[53] Zhai, J., Liu, J., Liu, B., Li, P., Meyers, B.C., Chen, X., Cao, X., and Ecker, J.R. (2008). Small RNA-directed epigenetic natural variation in Arabidopsis thaliana. PLoS Genet 4, e1000056.10.1371/journal.pgen.1000056
[54] Zhang, X., Segers, G.C., Sun, Q., Deng, F., and Nuss, D.L. (2008). Characterization of hypovirus-derived small RNAs generated in the chestnut blight fungus by an inducible DCL-2-dependent pathway. J Virol 82, 2613–2619 .10.1128/JVI.02324-07
[55] Zhou, H., Wang, H., Huang, L.F., Naylor, M., and Clifford, P. (2005). Heterogeneity in codon usages of sobemovirus genes. Arch Virol 150, 1591–1605 .10.1007/s00705-005-0510-4