Abstract
Plant microRNAs are crucial for post-transcriptional regulation of gene expression, with some of them particularly involved in regulating several disease resistance (R) genes. This study is a computational screening for microRNAs potentially involved in the regulation of disease resistance in bread wheat Triticum aestivum, through the genome and transcriptome of this crop species. We used plant miRNAs of the superfamily miR-482/2118 to find complementarities with the expressed sequence tags (ESTs) coding NBS-LRR proteins of the bread wheat. This analysis revealed a vast recognition potential, highlighting highly variable miRNA-mRNA hybridization schemes. Precursors of miR-2118/482 sequences that showed a potential for recognizing wheat NBS-LRR ESTs were used as input for similarity search in the T. aestivum transcriptome shotgun assemblies (TSA) database, enabling the identification of a couple of wheat TSA sequences (JV952948.1 and JV851699.1) that were predicted to adopt a stable miRNA/miRNA* duplex structure. The genomic regions corresponding to both predicted tae-miR-2118 genes were determined on wheat chromosomes 2DL and 5AS. The findings of the present study will contribute to a better understanding of R gene expression regulation in wheat.
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Allen, E., Xie, Z., Gustafson, A.M., Carrington, J.C. 2005. MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221.
Berezikov, E., Cuppen, E., Plasterk, R.H.A. 2006. Approaches to microRNA discovery. Nat. Genet. 38:S2–S7.
Berezikov, E., Chung, W.J., Willis, J., Cuppen, E., Lai, E.C. 2007. Mammalian mirtron genes. Mol. Cell. 28:328–336.
Carthew, R.W., Sontheimer, E.J. 2009. Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–655.
Curtis, B.C. 2002. Wheat in the World. In: Curtis, B.C. (ed.), Bread Wheat: Improvement and Production. Food and Agriculture Organisation of the United Nations (FAO). Rome, Italy. http://www.fao.org/docrep/006/y4011e/y4011e04.htm#bm04 (accessed 30.04.2016).
Dai, X., Zhao, P.X. 2011. PsRNATarget: a plant small RNA target analysis server. Nucleic Acids Res. 39:W155–W159.
de Vries, S., Kloesges, T., Rose, L.E. 2015. Evolutionarily dynamic, but robust, targeting of resistance genes by the miR482/2118 gene family in the Solanaceae. Genome Biol. Evol. 7:3307–3321.
Duan, J., Xia, C., Zhao, G., Jia, J., Kong, X. 2012. Optimizing de novo common wheat transcriptome assembly using short-read RNA-Seq data. BMC Genomics 13:392
Ellis, J.G., Jones, D.A. 2003. Plant disease resistance genes. In: Ezekowitz, R.A.B., Hoffmann, J.A. (eds), Innate Immunity. Humana Press Inc. Totowa, NJ, USA. pp. 27–45.
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., Carrington, J.C. 2007. High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2:e219.
Fahlgren, N., Carrington, J.C. 2010. Mirna target prediction in plants. Methods Mol. Biol. 592:51–57.
Jia, J., Zhao, S., Kong, X., Li, Y., Zhao, G., He, W., Appels, R., Pfeifer, M., Tao, Y., Zhang, X., Jing, R., Zhang, C., Ma, Y., Gao, L., Gao, C., Spannagl, M., Mayer, K.F.X., Li, D., Pan, S., Zheng, F., Hu, Q., Xia, X., Li, J., Liang, Q., Chen, J., Wicker, T., Gou, C., Kuang, H., He, G., Luo, Y., Keller, B., Xia, Q., Lu, P., Wang, J., Zou, H., Zhang, R., Xu, J., Gao, J., Middleton, C., Quan, Z., Liu, G., Wang, J., International Wheat Genome Sequencing Consortium, Yang, H., Liu, X., He, Z., Mao, L., Wang J. 2013. Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496:91–95.
Jones-Rhoades, M.W., Bartel, D.P. 2004. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell 14:787–799.
Kidner, C.A., Martienssen, R.A. 2004. Spatially restricted microRNA direct leaf polarity through ARGONAUTE1. Nature 428:81–84.
Li, F., Pignatta, D., Bendix, C., Brunkard, J.O., Cohn, M.M., Tung, J., Sun, H., Kumar, P., Baker, B. 2012. MicroRNA regulation of plant innate immune receptors. Proc. Natl Acad. Sci. USA 109:1790–1795.
Llave, C., Xie, Z., Kasschau, K.D., Carrington, J.C. 2002. Cleavage of scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297:2053–2056.
Lu, C., Jeong, D.H., Kulkarni, K., Pillay, M., Nobuta, K., German, R., Thatcher, S.R., Maher, C., Zhang, L., Ware, D., Liu, B., Cao, X., Meyers, B.C., Green, P.J. 2008. Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs). Proc. Natl Acad. Sci. USA 105:4951–4956.
Lund, E., Güttinger, S., Calado, A., Dahlberg, J.E., Kutay, U. 2004. Nuclear export of microRNA precursors. Science 303:95–98.
Marone, D., Russo, M.A., Laidò, G., De Leonardis, A.M., Mastrangelo, A.M. 2013. Plant nucleotide binding site–leucine-rich repeat (NBS–LRR) genes: active guardians in host defense responses. Int. J. Mol. Sci. 14:7302–7326.
Mendes, N.D., Freitas, A.T., Sagot, M.F. 2009. Current tools for the identification of miRNA genes and their targets. Nucleic Acids Res. 7:2419–2433.
Meyers, B.C., Kozik, A., Griego, A., Kuang, H., Michelmore, R.W. 2003. Genome-wide analysis of NBS–LRR–encoding genes in Arabidopsis. Plant Cell 15:809–834.
Nozawa, M., Miura, S., Nei, M. 2010. Origins and evolution of microRNA genes in Drosophila species. Genome Biol. Evol. 2:180–189.
Shivaprasad, P.V., Chen, H.M., Patel, K., Bond, D.M., Santos, B.A., Baulcombe, D.C. 2012. A microRNA superfamily regulates nucleotide binding site–leucine-rich repeats and other mRNAs. Plant Cell 24:859–874.
Wang, X.J., Reyes, J.L., Chua, N.H., Gaasterland, T. 2004. Prediction and identification of Arabidopsis thaliana microRNAs and their mRNA targets. Genome Biol. 5:R65.
Weber, H., Polen, T., Heuveling, J., Wendisch, V.F., Hengge, R. 2005. Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187:1591–1603.
Yang, G.D., Yan, K., Wu, B.J., Wang, Y.H., Gao, Y.X., Zheng, C.C. 2012. Genomewide analysis of intronic microRNAs in rice and Arabidopsis. J. Genet. 91:313–324.
Ying, S.Y., Chang, C.P., Lin, S.L. 2010. Intron-mediated RNA interference intronic microRNAs and applications. Methods Mol. Biol. 629:205–237.
Zhai, J., Jeong, D.H., De, Paoli, E., Park, S., Rosen, B.D., Li, Y., González, A.J., Yan, Z., Kitto, S.L., Grusak, M.A., Jackson, S.A., Stacey, G., Cook, D.R., Green, P.J., Sherrier, D.J., Meyers, B.C. 2011. MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev. 25:2540–2553.
Zhang, B.H., Pan, X.P., Wang, Q.L., Cobb, G.P., Anderson, T.A. 2005. Identification and characterization of new plant microRNAs using EST analysis. Cell Res. 15:336–360.
Zhang, B., Pan, X., Cobb, G.P., Anderson, T.A. 2006. Plant microRNA: a small regulatory molecule with big impact. Dev. Biol. 289:3–16.
Zhu, Q.H., Fan, L., Liu, Y., Xu, H., Llewellyn, D., Wilson, I. 2013. MiR482 regulation of NBS-LRR defense genes during fungal pathogen infection in cotton. PLoS ONE 8:e84390.
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This study was supported by the Tunisian Ministry of Higher Education and Scientific Research.
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Communicated by J. Kolmer
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Regulation of NBS-LRR Genes by MicroRNAs in Wheat: Computational Identification of Candidate MIR-2118 Genes and Evidence of Flexibility
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Khalfallah, Y., Bouktila, D., Habachi-Houimli, Y. et al. Regulation of NBS-LRR Genes by MicroRNAs in Wheat: Computational Identification of Candidate MIR-2118 Genes and Evidence of Flexibility. CEREAL RESEARCH COMMUNICATIONS 45, 83–92 (2017). https://doi.org/10.1556/0806.44.2016.049
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DOI: https://doi.org/10.1556/0806.44.2016.049