Skip to main content
Log in

MicroRNAs: potential target for genome editing in plants for traits improvement

  • Review Article
  • Published:
Indian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

The success of plant breeding for crop improvement is primarily dependent on effective utilization of coding and non-coding genetic elements. MicroRNAs are short non-coding RNAs transcribed from specific class of genes. These tiny RNAs regulate key biological processes in plants by targeting messenger RNAs for cleavage or translational inhibition. We herein describe the diverse functions of some of the well-studied miRNAs in different plant species and the possibility of using these miRNAs for crop improvement through genome editing. Some of the successful applications of genome editing of miRNAs are also described. This review presents key information on strategies and considerations to utilize miRNAs for genome editing with an example of rice. The major challenges of genome editing of miRNAs and the necessity of further studies to develop comprehensive knowledge of miRNA mediated gene regulatory networks and trait improvement, have been described in detail.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abdallah, N. A., Prakash, C. S., & McHughen, A. G. (2015). Genome editing for crop improvement: Challenges and opportunities. GM Crops & Food, 6, 183–205.

    Article  Google Scholar 

  • Abdel-Ghany, S. E., & Pilon, M. (2008). microRNA-mediated systemic downregulation of copper protein expression in response to low copper availability in Arabidopsis. Journal of Biological Chemistry, 283, 15932–15945.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agarwal, S., Mangrauthia, S. K., & Sarla, N. (2015). Expression profiling of iron deficiency responsive microRNAs and gene targets in rice seedlings of Madhukar x Swarna recombinant inbred lines with contrasting levels of iron in seeds. Plant and Soil, 396, 137.

    Article  CAS  Google Scholar 

  • Akdogan, G., Tufekci, E. D., Uranbey, S., & Unver, T. (2015). miRNA based drought regulation in wheat. Functional & Integrative Genomics, 16, 221–233.

    Article  CAS  Google Scholar 

  • Aukerman, M. J., & Sakai, H. (2003). Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell, 15, 2730–2741.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Axtell, M. J., & Bowman, J. L. (2008). Evolution of plant microRNAs and their targets. Trends in Plant Science, 13, 343–349.

    Article  CAS  PubMed  Google Scholar 

  • Baldrich, P., & Segundo, B. S. (2016). MicroRNAs in rice innate immunity. Rice, 9, 6.

    PubMed  Google Scholar 

  • Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281–297.

    Article  CAS  PubMed  Google Scholar 

  • Ben-Gera, H., & Ori, N. (2012). Auxin and LANCEOLATE affect leaf shape in tomato via different developmental processes. Plant Signalling Behaviour, 10, 1255–1257.

    Article  CAS  Google Scholar 

  • Bonnet, E., He, Y., Billiau, K., & Van de Peer, Y. (2010). TAPIR, a web server for the prediction of plant microRNA targets, including target mimics. Bioinformatics, 26, 1566–1568.

    Article  CAS  PubMed  Google Scholar 

  • Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y. Y., Sieburth, L., et al. (2008). Widespread translational inhibition by plant miRNAs and siRNAs. Science, 320, 1185–1190.

    Article  CAS  PubMed  Google Scholar 

  • Campo, S., Peris-Peris, C., Sire, C., Moreno, A. B., Donaire, L., Zytnicki, M., et al. (2013). Identification of a novel microRNAs (miRNA) from rice that targets an alternatively spliced transcript of the Nramp6 (Natural resistance-associated macrophage protein 6) gene involved in pathogen resistance. New Phytologist, 199, 212–227.

    Article  CAS  PubMed  Google Scholar 

  • Cermak, T., Baltes, N. J., Cegan, R., Zhang, Y., & Voytas, D. F. (2015). High frequency precision modification of the Tomato genome. Genome Biology, 16, 232.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chand, S. K., Nanda, S., & Joshi, R. K. (2016). Regulation of Fusarium oxysporum f. sp. cepae (FOC) infection in garlic (Allium sativum L.). Frontiers in Plant Sciences, 7, 258.

    Google Scholar 

  • Chang, H., Yi, B., Ma, R., Zhang, X., Chao, H., & Xi, Y. (2016). CRISPR/cas9, a novel genomic tool to knock down microRNAs in vitro and in vivo. Scientific Reports, 6, 22312.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chau, B. N., Xin, C., Hartner, J., Ren, S., Castano, A. P., Linn, G., et al. (2012). MicroRNA-21 promotes fibrosis of the kidney by silencing metabolic pathways. Science Translational Medicine, 4(121), ra18.

    Article  CAS  Google Scholar 

  • Chen, X. (2004). A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science, 303, 2022–2025.

    Article  CAS  PubMed  Google Scholar 

  • Chen, X. (2009). Small RNAs and their roles in plant development. Annual Reviews in Cell Developmental Biology, 25, 21–44.

    Article  CAS  Google Scholar 

  • Chen, H. M., Chen, L. T., Patel, K., Li, Y. H., Baulcombe, D. C., & Wu, S. H. (2010). 22-Nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proceedings of National Academy of Sciences U.S.A., 107, 15269–15274.

    Article  CAS  Google Scholar 

  • Chen, Y., Jiang, J., Song, A., Chen, S., Shan, H., Luo, H., et al. (2013). Ambient temperature enhanced freezing tolerance of Chrysanthmum dichrum CdICE1 Arabidopsis via miR398. BMC Biology, 11, 121.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chuck, G. S., Tobias, C., Sun, L., Kraemer, F., Li, C., Dibble, D., et al. (2011). Overexpression of the maize corngrass1 microRNA prevents flowering, improves digestibility, and increases starch content of switchgrass. Proceedings of National Academy of Sciences U.S.A., 108, 17550–17555.

    Article  CAS  Google Scholar 

  • Cui, L. G., Shan, J. X., Shi, M., Gao, J. P., & Lin, H. X. (2014). The miR156SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants. Plant Journal, 80, 1108–1117.

    Article  CAS  PubMed  Google Scholar 

  • Cui, N., Sun, X., Sun, M., Jia, B., Duanmu, H., Lv, D., et al. (2015). Overexpression of OsmiR156 k leads to reduced tolerance to cold stress in rice (Oryza sativa). Molecular Breeding, 35, 214.

    Article  CAS  Google Scholar 

  • Cuperus, J. T., Carbonell, A., Fahlgren, N., Garcia-Ruiz, H., Burke, R. T., Takeda, A., et al. (2010). Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nature Structural & Molecular Biology, 17, 997–1003.

    Article  CAS  Google Scholar 

  • Cuperus, J. T., Fahlgren, N., & Carrington, J. C. (2011). Evolution and functional diversification of MIRNA genes. Plant Cell, 23, 431–442.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding, D., Zhang, L., Wang, H., Liu, Z., Zhang, Z., & Zheng, Y. (2009). Differential expression of miRNAs in response to salt stress in maize roots. Annals of Botany, 103, 29–38.

    Article  CAS  PubMed  Google Scholar 

  • Dong, C. H., & Pei, H. (2014). Over-expression of miR397 improves plant tolerance to cold stress in Arabidopsis thaliana. Journal of Plant Biology, 57, 209–217.

    Article  CAS  Google Scholar 

  • Dugas, D. V., & Bartel, B. (2008). Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Molecular Biology, 67, 403–417.

    Article  CAS  PubMed  Google Scholar 

  • Fang, Y., & Spector, D. L. (2007). Identification of nuclear dicing bodies containing proteins for microRNAs biogenesis in living Arabidopsis plants. Current Biology, 17, 818–823.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fattash, I., Voss, B., Reski, R., Hess, W. R., & Frank, W. (2007). Evidence for the rapid expansion of microRNA-mediated regulation in early land plant evolution. BMC Plant Biology, 7, 13.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Felippes, F. F., Schneeberger, K., Dezulian, T., Huson, D. H., & Weigel, D. (2008). Evolution of Arabidopsis thaliana microRNAs from random sequences. RNA, 14, 2455–2459.

    Article  PubMed  CAS  Google Scholar 

  • Feng, H., Zhang, Q., Wang, Q., Wang, X., Liu, J., Li, M., et al. (2013). Target of tae-miR408, a chemocyanin-like protein gene (TaCLP1), plays positive roles in wheat response to high-salinity, heavy cupric stress and stripe rust. Plant Molecular Biology, 83, 433–443.

    Article  CAS  PubMed  Google Scholar 

  • Fu, C., Sunkar, R., Zhou, C., Shen, H., Zhang, J. Y., Matts, J., et al. (2012). Overexpression of miR156 in switchgrass (Panicum virgatum L.) results in various morphological alterations and leads to improved biomass production. Plant Biotechnology Journal, 10, 443–452.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii, H., Chiou, T. J., Lin, S. I., Aung, K., & Zhu, J. K. (2005). A miRNA involved in phosphate-starvation response in Arabidopsis. Current Biology, 15, 2038–2043.

    Article  CAS  PubMed  Google Scholar 

  • Gaj, T., Gersbach, C. A., & Barbas, C. F., 3rd. (2013). ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends in Biotechnology, 31, 397–405.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao, P., Bai, X., Yang, L., Lv, D., Li, Y., Cai, H., et al. (2010). Over-expression of osa-MIR396c decreases salt and alkali stress tolerance. Planta, 231, 991–1001.

    Article  CAS  PubMed  Google Scholar 

  • Georges, F., & Ray, H. (2017). Genome editing of crops: A renewed opportunity for food security. GM Crops Food, 8, 1–12.

    Article  PubMed  Google Scholar 

  • Gou, J. Y., Felippes, F. F., Liu, C. J., Weigel, D., & Wang, J. W. (2011). Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell, 23, 1512–1522.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gregory, B. D., O’Malley, R. C., Lister, R., Urich, M. A., Tonti-Filippini, J., Chen, H., et al. (2008). A link between RNA metabolism and silencing affecting Arabidopsis development. Developmental Cell, 14, 854–866.

    Article  CAS  PubMed  Google Scholar 

  • Guan, Q., Lu, X., Zeng, H., Zhang, Y., & Zhu, J. (2013). Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant Journal, 74, 840–851.

    Article  CAS  PubMed  Google Scholar 

  • Gupta, O. P., Meena, N. L., Sharma, I., & Sharma, P. (2014). Differential regulation of microRNAs in response to osmotic, salt and cold stresses in wheat. Molecular Biology Reports, 41, 4623–4629.

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez, L., Bussell, J. D., Pacurar, D. I., Schwambach, J., Pacurar, M., & Bellini, C. (2009). Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell, 21, 3119–3132.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haft, D. H., Selengut, J., Mongodin, E. F., & Nelson, K. E. (2005). A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Computational Biology, 1, e60.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hajyzadeh, M., Turktas, M., Khawar, K. M., & Unver, T. (2015). miR408 overexpression causes increased drought tolerance in chickpea. Gene, 555, 186–193.

    Article  CAS  PubMed  Google Scholar 

  • Hanemian, M., Barlet, X., Sorin, C., Yadeta, K. A., Keller, H., Favery, B., et al. (2016). Arabidopsis CLAVATA1 and CLAVATA2 receptors contribute to Ralstonia solanacearum pathogenicity through a miR169-dependent pathway. New Phytologist, 211, 502–515.

    Article  CAS  PubMed  Google Scholar 

  • He, H., He, L., & Gu, M. (2014). Role of microRNAs in aluminium stress in plants. Plant Cell Reports, 33, 831–836.

    Article  CAS  PubMed  Google Scholar 

  • Hendelman, A., Buxdorf, K., Stav, R., Kravchik, M., & Arazi, T. (2012). Inhibition of lamina outgrowth following Solanum lycopersicum AUXIN RESPONSE FACTOR 10 (SlARF10) derepression. Plant Molecular Biology, 78, 561–576.

    Article  CAS  PubMed  Google Scholar 

  • Hsieh, L., Lin, S., Shih, A., Chen, J., Lin, W., Tseng, C., et al. (2009). Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiology, 151, 2120–2132.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu, R., Huffaker, T. B., Kagele, D. A., Runtsch, M. C., Bake, E., Chaudhuri, A. A., et al. (2013). MicroRNA-155 confers encephalogenic potential to Th17 cells by promoting effector gene expression. Journal of Immunology, 190, 5972–5980.

    Article  CAS  Google Scholar 

  • Huang, S. Q., Xiang, A. L., Che, L. L., Chen, S., Hui, L., Song, J. B., et al. (2010). A set of miRNAs from Brassica napus in response to sulfate-deficiency and cadmium stress. Plant Biotechnology Journal, 8, 887–899.

    Article  CAS  PubMed  Google Scholar 

  • Huijser, P., & Schmid, M. (2011). The control of developmental phase transitions in plants. Development, 138, 4117–4129.

    Article  CAS  PubMed  Google Scholar 

  • Jagadeeswaran, G., Saini, A., & Sunkar, R. (2009). Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta, 229, 1009–1014.

    Article  CAS  PubMed  Google Scholar 

  • Jia, X., Wang, W. X., Ren, L., Chen, Q.-J., Mendu, V., Willcut, B., et al. (2009). Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Molecular Biology, 71, 51–59.

    Article  CAS  PubMed  Google Scholar 

  • Jiao, Y., Wang, Y., Xue, D., Wang, J., Yan, M., Liu, G., et al. (2010). Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nature Genetics, 42, 541–544.

    Article  CAS  PubMed  Google Scholar 

  • Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., & Charpentier, E. (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337, 816–821.

    Article  CAS  PubMed  Google Scholar 

  • Jing, W., Zhang, X., Sun, W., Hou, X., Yao, Z., & Zhu, Y. (2015). CRISPR/CAS9-mediated genome editing of miR-155 inhibits proinflammatory cytokine production by RAW264.7 cells. BioMed Research International, 2015, 326042.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jones-Rhoades, M. W., & Bartel, D. P. (2004). Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Molecular Cell, 14, 787–799.

    Article  CAS  PubMed  Google Scholar 

  • Jones-Rhoades, M. W., Bartel, D. P., & Bartel, B. (2006). MicroRNAs and their regulatory roles in plants. Annual Reviews in Plant Biology, 57, 19–53.

    Article  CAS  Google Scholar 

  • Jovanovic, Z., Stanisavljevic, N., Mikic, A., Radovic, S., & Maksimovic, V. (2014). Water deficit down-regulates miR398 and miR408 in pea (Pisum sativum L.). Plant Physiology and Biochemistry, 83, 26–31.

    Article  CAS  PubMed  Google Scholar 

  • Kaur, S., Sharma, B., Gupta, A. K., Kaur, S., & Kaur, J. (2014). Nodule metabolism in cold stress tolerant and susceptible chickpea cultivars. Symbiosis, 64, 33–42.

    Article  CAS  Google Scholar 

  • Khraiwesh, B., Arif, M. A., Seumel, G. I., Ossowski, S., Weigel, D., Reski, R., et al. (2010). Transcriptional control of gene expression by microRNAs. Cell, 140, 111–122.

    Article  CAS  PubMed  Google Scholar 

  • Khraiwesh, B., Zhu, J. K., & Zhu, J. (2012). Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochimica et Biophysica Acta, 1819, 137–148.

    Article  CAS  PubMed  Google Scholar 

  • Kim, J., Lee, J., Kim, W., Jung, H., Huijser, P., & Ahn, J. (2012). The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Plant Physiology, 159, 461–478.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knauer, S., Holt, A. L., Rubio-Somoza, I., Tucker, E. J., Hinze, A., Pisch, M., et al. (2013). A protodermal miR394 signal defines a region of stem cell competence in the Arabidopsis shoot meristem. Developmental Cell, 24, 1–8.

    Article  CAS  Google Scholar 

  • Kong, W. W., & Yang, Z. M. (2010). Identification of iron-deficiency responsive microRNA genes and cis-elements in Arabidopsis. Plant Physiology and Biochemistry, 48, 153–159.

    Article  CAS  PubMed  Google Scholar 

  • Koyama, T., Furutani, M., Tasaka, M., & Ohme-Takagi, M. (2007). TCP transcription factors control the morphology of shoot lateral organs via negative regulation of the expression of boundary specific genes in Arabidopsis. Plant Cell, 19, 473–484.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koyama, T., Mitsuda, N., Seki, M., Shinozaki, K., & Ohme-Takagi, M. (2010). TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell, 22, 3574–3588.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kozomara, A., & Griffiths-Jones, S. (2011). miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Research, 39, D152–D157.

    Article  CAS  PubMed  Google Scholar 

  • Kurata, J., & Lin, R.-J. (2015). TALEN-engineered human cell lines with microRNAs-21 null mutations. RNA & Disease, 2, e727.

    Google Scholar 

  • Laubinger, S., Sachsenberg, T., Zeller, G., Busch, W., Lohmann, J. U., Rätsch, G., et al. (2008). Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Proceedings of National Academy of Science U.S.A., 105, 8795–8800.

    Article  CAS  Google Scholar 

  • Lee, R. C., Feinbaum, R. L., & Ambros, V. (1993). The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 75, 843–854.

    Article  CAS  PubMed  Google Scholar 

  • Lee, D. K., Kim, H. I., Jang, G., Chung, P. J., Jeong, J. S., Kim, Y. S., et al. (2015). The NF-YA transcription factor OsNF-YA7 confers drought stress tolerance of rice in an abscisic acid independent manner. Plant Science, 241, 199–210.

    Article  CAS  PubMed  Google Scholar 

  • Leyva-Gonzalez, M. A., Ibarra-Laclette, E., Cruz-Ramirez, A., & Herrera Estrella, L. (2012). Functional and transcriptome analysis reveals an acclimatization strategy for abiotic stress tolerance mediated by Arabidopsis NFYA family members. PLoS One, 7, e48138.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, H., Dong, Y., Yin, H., Wang, N., Yang, J., Liu, X., et al. (2011). Characterization of the stress associated microRNAs in Glycine max by deep sequencing. BMC Plant Biology, 11, 170.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li, Y., Lu, Y. G., Shi, Y., Wu, L., Xu, Y. J., Huang, F., et al. (2014). Multiple rice microRNAs are involved in immunity against the blast fungus Magnaporthe oryzae. Plant Physiology, 164, 1077–1092.

    Article  CAS  PubMed  Google Scholar 

  • Li, J. F., Norville, J. E., Aach, J., McCormack, M., Zhang, D., Bush, J., et al. (2013). Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nature Biotechnology, 31, 688–691.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, W., Oono, Y., Zhu, J., He, X., Wu, J., Iida, K., et al. (2008). The Arabidopsis NFYA5 transcription factors regulated transcriptionally and post-transcriptionally to promote drought resistance. Plant Cell, 20, 2238–2251.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, W., Wang, T., Zhang, Y., & Li, Y. (2016). Over-expression of soybean miR172c confers tolerance to water deficit and salt stress, but increases ABA sensitivity in transgenic Arabidopsis thaliana. Journal of Experimental Botany, 67, 175–194.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., Zhang, Q., Zhang, J., Wu, L., Qi, Y., & Zhou, J. M. (2010). Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiology, 152, 2222–2231.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, Y., Zhao, S.-L., Li, J.-L., Hu, X.-H., Wang, H., Cao, X.-L., et al. (2017). Osa-miR169 negatively regulates rice immunity against the blast fungus Magnaporthe oryzae. Frontiers in Plant Sciences, 8, 2.

    Google Scholar 

  • Liang, G., He, H., & Yu, D. (2012). Identification of nitrogen starvation responsive microRNAs in Arabidopsis thaliana. PLoS One, 7, e48951.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, W.-T., Chen, P.-W., Chen, L.-C., Yang, C.-C., Chen, S.-Y., Huang, G.-F., et al. (2017a). Suppressive effect of microRNA319 expression on rice plant height. Theoretical and Applied Genetics, 130, 1507–1518.

    Article  CAS  PubMed  Google Scholar 

  • Liu, X., Huang, J., Wang, Y., Khanna, K., Xie, Z., Owen, H. A., et al. (2010). The role of floral organs in carpels, an Arabidopsis loss-of-function mutation in microRNA160a, in organogenesis and the mechanism regulating its expression. Plant Journal, 62, 416–428.

    Article  PubMed  CAS  Google Scholar 

  • Liu, P. P., Montgomery, T. A., Fahlgren, N., Kasschau, K. D., Nonogaki, H., & Carrington, J. C. (2007). Epression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. The Plant Journal, 52(1), 133–146.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H. H., Tian, X., Li, Y. J., Wu, C. A., & Zheng, C. C. (2008). Microarray based analysis of stress regulated microRNAs in Arabidopsis thaliana. RNA, 14, 836–843.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, X., Yang, L., Zhou, X., Zhou, M., Lu, Y., Ma, L., et al. (2013). Transgenic wheat expressing Thinopyrum intermedium MYB transcription factor TiMYB2R-1 shows enhanced resistance to the take-all disease. Journal of Experimental Botany, 64, 2243–2253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, M., Yu, H., Zhao, G., Huang, Q., Lu, Y., & Ouyang, B. (2017b). Profiling of drought-responsive microRNA and mRNA in tomato using high-throughput sequencing. BMC Genomics, 18, 481.

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu, Q., Zhang, Y. C., Wang, C. Y., Luo, Y. C., Huang, Q. J., et al. (2009). Expression analysis of phytohormone-regulated microRNAs in rice, implying their regulation roles in plant hormone signaling. FEBS Letters, 583, 723–728.

    Article  CAS  PubMed  Google Scholar 

  • Llave, C., Kasschau, K. D., Rector, M. A., & Carrington, J. C. (2002). Endogenous and silencing associated small RNAs in plants. Plant Cell, 14, 1605–1619.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luan, M., Xu, M., Lu, Y., Zhang, L., Fan, Y., & Wang, L. (2015). Expression of zma-miR169 miRNAs and their target ZmNF-YA genes in response to abiotic stress in maize leaves. Gene, 555, 178–185.

    Article  CAS  PubMed  Google Scholar 

  • Luan, M., Xu, M., Lu, Y., Zhang, Q., Zhang, L., & Zhang, C. (2014). Family-wide survey of miR169 s and NF-YAs and their expression profiles response to abiotic stress in maize roots. PLoS One, 9, e91369.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lv, D. K., Bai, X., Li, Y., Ding, X. D., Ge, Y., Cai, H., et al. (2010). Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene, 459, 39–47.

    Article  CAS  PubMed  Google Scholar 

  • Mallory, A. C., Bartel, D. P., & Bartel, B. (2005). MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential foe proper development and modulates expression of early auxin response genes. Plant Cell, 17, 1360–1375.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mallory, A. P., & Vaucheret, H. (2006). Functions of microRNAs and related small RNAs in plants. Nature Genetics, 38, S31–S36.

    Article  CAS  PubMed  Google Scholar 

  • Mangrauthia, S. K., Agarwal, S., Sailaja, B., Madhav, M. S., & Voleti, S. R. (2013). MicroRNAs and their role in salt stress response in plants. In P. Ahmad, M. M. Azooz, & M. N. V. Prasad (Eds.), Salt stress in plants (pp. 15–46). Springer: New York.

    Chapter  Google Scholar 

  • Mangrauthia, S. K., Bhogireddy, S., Agarwal, S., Prasanth, V. V., Voleti, S. R., Neelamraju, S., et al. (2017). Genome-wide changes in microRNA expression during short and prolonged heat stress and recovery in contrasting rice cultivars. Journal of Experimental Botany, 68, 2399–2412.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mantovani, R. (1999). The molecular biology of the CCAAT-binding factor NF-Y. Gene, 239, 15–27.

    Article  CAS  PubMed  Google Scholar 

  • Meyers, B. C., Axtell, M. J., Bartel, B., Bartel, D. P., Baulcombe, D., et al. (2008). Criteria for annotation of plant microRNAs. Plant Cell, 20, 3186–3190.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitsuda, N., & Ohme-Takagi, M. (2009). Functional analysis of transcription factors in Arabidopsis. Plant Cell Physiology, 50, 1232–1248.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miura, K., Ikeda, M., Matsubara, A., Song, X. J., Ito, M., Asano, K., et al. (2010). OsSPL14 promotes panicle branching and higher grain productivity in rice. Nature Genetics, 42, 545–549.

    Article  CAS  PubMed  Google Scholar 

  • Molesini, B., Pii, Y., & Pandolfini, T. (2012). Fruit improvement using intragenesis and artificial microRNA. Trends in Biotechnology, 30, 80–88.

    Article  CAS  PubMed  Google Scholar 

  • Moxon, S., Jing, R., Szittya, G., Schwach, F., Pilcher, R. L. R., Moulton, V., et al. (2008). Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening. Genome Research, 18, 1602–1609.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muhammad, A., Gruber, M. Y., Wall, K., & Hannoufa, A. (2017). An insight into microRNA156 role in salinity stress responses of Alfalfa. Frontiers in Plant Sciences, 8, 356.

    Google Scholar 

  • Mutum, R. D., Balyanm, S. C., Kansal, S., Agarwal, P., Kumar, S., Kumar, M., et al. (2013). Evolution of variety-specific regulatory schema for expression of osa-miR408 in indica rice varieties under drought stress. FEBS Journal, 280, 1717–1730.

    Article  CAS  PubMed  Google Scholar 

  • Nag, A., King, S., & Jack, T. (2009). miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proceedings of National Academy of Science U.S.A., 106, 22534–22539.

    Article  CAS  Google Scholar 

  • Nath, U., Crawford, B. C., Carpenter, R., & Coen, E. (2003). Genetic control of surface curvature. Science, 299, 1404–1407.

    Article  CAS  PubMed  Google Scholar 

  • Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., & Estelle, M. (2006). A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science, 312, 436–439.

    Article  CAS  PubMed  Google Scholar 

  • Nemudryi, A. A., Valetdinova, K. R., Medvedev, S. P., & Zakian, S. M. (2014). TALEN and CRISPR/Cas genome editing systems: Tools of discovery. Acta Naturae, 6, 19–40.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ni, Z., Hu, Z., Jiang, Q., & Zhang, H. (2012). Overexpression of gma-MIR394a confers tolerance to drought in transgenic Arabidopsis thaliana. Biochemistry & Biophysics Research Communications, 19, 330–335.

    Article  CAS  Google Scholar 

  • Nizampatnam, N. R., Schreier, S. J., Damodaran, S., Adhikari, S., & Subramanian, S. (2015). microRNAs 160 dictates stage-specific auxin and cytokinin sensitivities and directs soybean nodule development. The Plant Journal, 84, 140–153.

    Article  CAS  PubMed  Google Scholar 

  • Ori, N., Cohen, A. R., Etzioni, A., Brand, A., Yanai, O., Shleizer, S., et al. (2007). Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nature Genetics, 39, 787–791.

    Article  CAS  PubMed  Google Scholar 

  • Ozhuner, E., Eldem, V., Ipek, A., Okay, S., Sakcali, S., Zhang, B., et al. (2013). Boron stress responsive microRNAs and their targets in barley. PLoS One, 8, e59543.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palatnik, J. F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J. C., et al. (2003). Control of leaf morphogenesis by microRNAs. Nature, 425, 257–263.

    Article  CAS  PubMed  Google Scholar 

  • Palatnik, J. F., Wollmann, H., Schommer, C., Schwab, R., Boishouvier, J., et al. (2007). Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Developmental Cel, 1(3), 115–125.

    Article  CAS  Google Scholar 

  • Pan, L., Zhao, H., Yu, Q., Bai, L., & Dong, L. (2017). miR397/Laccase gene mediated network improves tolerance to fenoxaprop-p-ethyl in Beckmannia syzigachne and Oryza sativa. Frontiers in Plant Sciences, 8, 879.

    Article  Google Scholar 

  • Pant, B. D., Buhtz, A., Kehr, J., & Scheible, W. R. (2008). MicroRNA399 is a long distance signal for the regulation of plant phosphate homeostasis. Plant Journal, 53, 731–738.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park, W., Li, J., Song, R., Messing, J., & Chen, X. (2002). CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Current Biology, 12, 1484–1495.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pashkovskiy, P. P., & Ryazansky, S. S. (2013). Biogenesis, evolution and functions of plant microRNAs. Biochemistry, 78, 627–637.

    CAS  PubMed  Google Scholar 

  • Paul, S., Datta, S. K., & Datta, K. (2015). miRNA regulation of nutrient homeostasis in plants. Frontiers in Plant Science, 6, 232.

    Article  PubMed  PubMed Central  Google Scholar 

  • Poethig, R. S. (2013). Vegetative phase change and shoot maturation in plants. Current Topics in Developmental Biology, 105, 125–152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian, M., Ni, J., Niu, Q., Bai, S., Bao, L., Li, J., et al. (2017). Response of miR156-SPL module during the red peel coloration of bagging-treated Chinese Sand Pear (Pyrus pyrifolia Nakai). Frontiers in Physiology, 8, 550.

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiao, M., Zhao, Z., Song, Y., Liu, Z., Cao, L., Yu, Y., et al. (2012). Proper regeneration from in vitro cultured Arabidopsis thaliana requires the microRNA-directed action of an auxin response factor. Plant Journal, 71, 14–22.

    Article  CAS  PubMed  Google Scholar 

  • Qu, B., He, X., Wang, J., Zhao, Y., Teng, W., Shao, A., et al. (2015). A wheat CCAAT box-binding transcription factor increases the grain yield of wheat with less fertilizer input. Plant Physiology, 167, 411–423.

    Article  CAS  PubMed  Google Scholar 

  • Rhoades, M. W., Reinhart, B. J., Lim, L. P., Burge, C. B., Bartel, B., & Bartel, D. P. (2002). Prediction of plant microRNA targets. Cell, 110, 513–520.

    Article  CAS  PubMed  Google Scholar 

  • Roy, S., Khanna, S., Hussain, S. R. A., Biswas, S., Azad, A., Rink, C., et al. (2009). MicroRNA expression in response to murine myocardial infarction: miR-21 regulates fibroblast metalloprotease-2 via phosphatase and tensin homologue. Cardiovascular Research, 82, 21–29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schommer, C., Bresso, E. G., Spinelli, S. V., & Palatnik, J. F. (2012). Role of microRNAs miR319 in plant development. In R. Sunkar (Ed.), MicroRNAs in plant development and stress responses, signalling and communication in plants (pp. 29–47). Berlin: Springer.

    Chapter  Google Scholar 

  • Schommer, C., Palatnik, J. F., Aggarwal, P., Chetelat, A., Cubas, P., Farmer, E. E., et al. (2008). Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biology, 6, e230.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schwab, R., Ossowski, S., Riester, M., Warthmann, M., & Weigel, D. (2006). Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell, 18, 1121–1133.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwab, R., Palatnik, J. F., Riester, M., Schommer, C., Schmid, M., & Weigel, D. (2005). Specific effects of microRNAs on the plant transcriptome. Developmental Cell, 8, 517–527.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shriram, V., Kumar, V., Devarumath, R., Khare, T. S., & Wani, S. H. (2016). MicroRNAs as potential targets for abiotic stress tolerance in plants. Frontiers in Plant Science, 7, 817.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shu, Y. J., Liu, Y., Li, W., Song, L. L., Zhang, J., & Guo, C. H. (2016). Genome wide investigation of microRNAs and their targets in response to freezing stress in Medicago sativa L., based on high-throughput sequencing. G3 (Bethesda), 6, 755–765.

    Article  Google Scholar 

  • Song, J. B., Gao, S., Sun, D., Li, H., Shu, X. X., & Yang, Z. M. (2013). miR394 and LCR are involved in Arabidopsis salt and drought stress responses in an abscisic acid independent manner. BMC Plant Biology, 13, 210.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Song, J. B., Gao, S., Wang, Y., Li, B. W., Zhang, Y. L., & Yang, Z. M. (2016a). miR394 and its target gene LCR are involved in cold stress response in Arabidopsis. Plant Gene, 5, 56–64.

    Article  CAS  Google Scholar 

  • Song, J. B., Huang, S. Q., Dalmay, T., & Yang, Z. M. (2012). Regulation of leaf morphology by microRNA394 and its target LEAF CURLING RESPONSIVENESS. Plant Cell Physiology, 53, 1283–1294.

    Article  CAS  PubMed  Google Scholar 

  • Song, G., Jia, M., Chen, K., Kong, X., Khattak, B., Xie, C., et al. (2016b). CRISPR/Cas9: a powerful tool for crop genome editing. Crop Journal, 4, 75–82.

    Article  Google Scholar 

  • Sun, G., Stewart, C. N., Jr., Xiao, P., & Zhang, B. (2012). MicroRNA expression analysis in the cellulosic biofuel crop switchgrass (Panicum virgatum) under abiotic stress. PLoS One, 7, e32017.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunkar, R., Chinnusamy, V., Zhu, J., & Zhu, J. K. (2007). Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends in Plant Science, 12, 301–309.

    Article  CAS  PubMed  Google Scholar 

  • Sunkar, R., Kapoor, A., & Zhu, J. K. (2006). Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell, 18, 2051–2065.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunkar, R., Li, Y. F., & Jagadeeswaran, G. (2012). Functions of microRNAs in plant stress responses. Trends in Plant Science, 17, 196–203.

    Article  CAS  PubMed  Google Scholar 

  • Sunkar, R., & Zhu, J. K. (2004). Novel and stress-regulated micro RNAs and other small RNAs from Arabidopsis. Plant Cell, 16, 2001–2019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szostak, J. W., Orr-Weaver, T. L., Rothstein, R. J., & Stahl, F. W. (1983). The double-strand-break repair model for recombination. Cell, 33, 25–35.

    Article  CAS  PubMed  Google Scholar 

  • Takada, S., Sato, T., Ito, Y., Yamashita, S., Kato, T., Kawasumi, M., et al. (2013). Targeted gene deletion of miRNAs in mice by TALEN system. PLoS One, 8, e76004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Talmor-Neiman, M., Stav, R., Frank, W., Voss, B., & Arazi, T. (2006). Novel microRNAs and intermediates of micro-RNA biogenesis from moss. Plant Journal, 47, 25–37.

    Article  CAS  PubMed  Google Scholar 

  • Tan, W. S., Carlson, D. F., Walton, M. W., Fahrenkrug, S. C., & Hackett, P. B. (2012). Precision editing of large animal genomes. Advances in Genetics, 80, 37–97.

    CAS  PubMed  Google Scholar 

  • Tang, J., & Chu, C. (2017). MicroRNAs in crop improvement: fine-tuners for complex traits. Nature Plants, 3, 17077.

    Article  PubMed  Google Scholar 

  • Thiebaut, F., Rojas, C. A., Almeida, K. L., Grativol, C., Domiciano, C. G., et al. (2012). Regulation of miR319 during cold stress in sugarcane. Plant Cell Environment, 35, 502–512.

    Article  CAS  Google Scholar 

  • Thum, T., Gross, C., Fiedler, J., Fischer, T., Kissler, S., Bussen, M., et al. (2008). MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature, 456, 980–984.

    Article  CAS  PubMed  Google Scholar 

  • Trindade, I., Capitao, C., Dalmay, T., Fevereiro, M. P., & Santos, D. M. (2010). miR398 and miR408 are upregulated in response to water deficit in Medicago truncatula. Planta, 231, 705–716.

    Article  CAS  PubMed  Google Scholar 

  • Turner, M., Nizampatnam, N. R., Baron, M., Coppin, S., Damodaran, S., Adhikari, et al. (2013). Ectopic expression of miR160 results in auxin hypersensitivity, cytokinin hyposensitivity, and inhibition of symbiotic nodule development in soybean. Plant Physiology, 162, 2042–2055.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vazquez, F. (2006). Arabidopsis endogenous small RNAs: highways and byways. Trends in Plant Science, 11, 460–468.

    Article  CAS  PubMed  Google Scholar 

  • Vazquez, F., Blevins, T., Ailhas, J., Boller, T., & Meins, F., Jr. (2008). Evolution of Arabidopsis MIR genes generates novel microRNA classes. Nucleic Acids Research, 36, 6429–6438.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voinnet, O. (2009). Origin, biogenesis, and activity of plant microRNAs. Cell, 136, 669–687.

    Article  CAS  PubMed  Google Scholar 

  • Voytas, D. F. (2013). Plant genome engineering with sequence-specific nucleases. Annual Reviews in Plant Biology, 64, 327–350.

    Article  CAS  Google Scholar 

  • Wang, J. W. (2014). Regulation of flowering time by the miR156-mediated age pathway. Journal Experimental Botany, 65, 4723–4730.

    Article  CAS  Google Scholar 

  • Wang, H., La Russa, M., & Qi, L. S. (2016a). CRISPR/Cas9 in genome editing and beyond. Annual Reviews in Biochemistry, 85, 227–264.

    Article  CAS  Google Scholar 

  • Wang, F., Polydore, S., & Axtell, M. J. (2015). More than meets the eye? Factors that affect target selection by plant miRNAs and heterochromatic siRNAs. Current Opinions in Plant Biology, 27, 118–124.

    Article  CAS  Google Scholar 

  • Wang, S.-T., Sun, X.-I., Hoshino, Y., Yu, Y., Jia, B., et al. (2014). MicroRNA319 positively regulates cole tolerance by targeting OsPCF6 and OsTCP21 in rice (Oryza sativa L.). PLoS One, 9, e91357.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang, H., & Wang, H. (2015). The miR156/SPL module, a regulatory hub and versatile toolbox, gears up crops for enhanced agronomic traits. Molecular Plant, 8, 677–688.

    Article  CAS  PubMed  Google Scholar 

  • Wang, F., Wang, C., Liu, P., Lei, C., Hao, W., Gao, Y., et al. (2016b). Enhanced rice blast resistance by CRISPR/Cas9-targeted mutagenesis of the ERF transcription factor gene OsERF922. PLoS One, 11, e0154027.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang, J. W., Wang, L. J., Mao, Y. B., Cai, W. J., Xue, H. W., & Chen, X. Y. (2005). Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell, 17, 2204–2216.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, S., Wu, K., Yuan, Q., Liu, X., Liu, Z., Lin, X., et al. (2012). Control of grain size, shape and quality by OsSPL16 in rice. Nature Genetics, 44, 950–954.

    Article  CAS  PubMed  Google Scholar 

  • Warthmann, N., Chen, H., Ossowski, S., Weigel, D., & Herve, P. (2008). Highly specific gene silencing by artificial miRNAs in rice. PLoS One, 3, e1829.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Weigel, D., Ahn, J. H., Blazquez, M. A., Borevitz, J. O., Christensen, S. K., Fankhauser, C., et al. (2000). Activation tagging in Arabidopsis. Plant Physiology, 122, 1003–1013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, L., Zhang, Q., Zhou, H., Ni, F., Wu, X., & Qi, Y. (2009). Rice MicroRNA effector complexes and targets. Plant Cell, 21, 3421–3435.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie, Z., Kasschau, K. D., & Carrington, J. C. (2003). Negative feedback regulation of Dicer-Like1 in Arabidopsis by microRNA-guided mRNA degradation. Current Biology, 13, 784–789.

    Article  CAS  PubMed  Google Scholar 

  • Xie, K., Shen, J., Hou, X., Yao, J., Li, X., Xiao, J., et al. (2012). Gradual increase of miR156 regulates temporal expression changes of numerous genes during leaf development in rice. Plant Physiology, 158, 1382–1394.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie, K., Wu, C., & Xiong, L. (2006). Genomic organization, differential expression, and interaction of Squamosa promoter-binding- like transcription factors and microRNA156 in rice. Plant Physiology, 142, 280–293.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie, K., & Yang, Y. (2013). RNA-guided genome editing in plants using CRISPR-Cas system. Molecular Plant, 6, 1975–1983.

    Article  CAS  PubMed  Google Scholar 

  • Xie, F., Ye, L., Chang, J. C., Beyer, A. I., Wang, J., Muench, M. O., et al. (2014). Seamless gene correction of β-thalassemia mutations in patient-specific iPSCs using CRISPR/Cas9 and piggyBac. Genome Research, 24, 1526–1533.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamasaki, H., Abdel-Ghany, S. E., Cohu, C. M., Kobayashi, Y., Shikanai, T., & Pilon, M. (2007). Regulation of copper homeostasis by micro-RNA in Arabidopsis. Journal of Biological and Chemistry, 282, 16369–16378.

    Article  CAS  Google Scholar 

  • Yanai, O., Shani, E., Russ, D., & Ori, N. (2011). Gibberellin partly mediates LANCEOLATE activity in tomato. Plant Journal, 68, 571–582.

    Article  CAS  PubMed  Google Scholar 

  • Yang, C. H., Li, D. Y., Mao, D. H., Liu, X., Ji, C. J., et al. (2013). Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.). Plant Cell Environment, 36, 2207–2218.

    Article  CAS  Google Scholar 

  • Yin, K., Gao, C., & Qiu, J.-L. (2017). Progress and prospects in plant genome editing. Nature Plants, 3, 17107.

    Article  CAS  PubMed  Google Scholar 

  • Yu, X., Wang, H., Lu, Y., de Ruiter, M., Cariason, M., Prins, M., et al. (2012). Identification of conserved and novel microRNAs that are responsive to heat stress in Brassica rapa. Journal of Experimental Botany, 63, 1025–1038.

    Article  CAS  PubMed  Google Scholar 

  • Zamore, P. D., & Haley, B. (2005). Ribo-genome: the big world of small RNAs. Science, 309, 1519–1524.

    Article  CAS  PubMed  Google Scholar 

  • Zhai, J., Jeong, D. H., De Paoli, E., Park, S., Rosen, B. D., et al. (2011). MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes & Development, 25, 2540–2553.

    Article  CAS  Google Scholar 

  • Zhang, B. (2015). MicroRNA: a new target for improving plant tolerance to abiotic stress. Journal of Experimental Botany, 66, 1749–1761.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, H., & Li, L. (2013). SQUAMOSA promoter binding protein-like7 regulated microRNA408 is required for vegetative development in Arabidopsis. Plant Journal, 74, 98–109.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, R., Marshall, D., Bryan, G. J., & Hornyik, C. (2013a). Identification and characterization of miRNA transcriptome in potato by high-throughput sequencing. PLoS One, 8, e57233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, B., Pan, X., & Anderson, T. A. (2006). Identification of 188 conserved maize microRNAs and their targets. FEBS Letters, 580, 3753–3762.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, B., & Wang, Q. (2015). MicroRNA-Based Biotechnology for Plant Improvement. Journal of Cell Physiology, 230, 1–15.

    Article  CAS  Google Scholar 

  • Zhang, Y. C., Yu, Y., Wang, C. Y., Li, Z. Y., Liu, Q., et al. (2013b). Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nature Biotechnology, 31, 848–852.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, H., Zhao, X., Li, J., Cai, H., Deng, X. W., & Li, L. (2014). MicroRNA408 is critical for the HY5-SPL7 gene network that mediates the coordinated response to light and copper. Plant Cell, 26, 4933–4953.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, X., Zou, Z., Gong, P., Zhang, J., Ziaf, K., Li, H., et al. (2011a). Over-expression of microRNA169 confers enhanced drought tolerance to tomato. Biotechnology Letters, 33, 403–409.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, X., Zou, Z., Zhang, J., Zhang, Y., Han, Q., Hu, T., et al. (2011b). Overexpression of sly-miR156a in tomato results in multiple vegetative and reproductive trait alterations and partial phenocopy of the sft mutant. FEBS Letters, 585, 435–439.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, M., Ding, H., Zhu, J. K., Zhang, F., & Li, W. X. (2011). Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytologist, 190, 906–915.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, X. Y., Hong, P., Wu, J. Y., Chen, X. B., Ye, X. G., Pan, Y. Y., et al. (2016). The tae-miR408-mediated control of TaTOC1 genes transcription is required for the regulation of heading time in wheat. Plant Physiology, 170, 1578–1594.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, B. T., Liang, R. Q., Ge, L. F., Li, W., Xiao, H. S., Lin, H. X., et al. (2007). Identification of drought-induced microRNAs in rice. Biochemical and Biophysical Research Communications, 354, 585–590.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, J., Deng, K., Cheng, Y., Zhong, Z., Tian, L., Tang, X., et al. (2017). CRISPR-Cas9 based genome editing reveals new insights into microRNAs function and regulation in rice. Frontiers in Plant Science, 8, 1598.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou, M., Gu, L. F., Li, P. C., Song, X. W., Wei, L. Y., Chen, Z. Y., et al. (2010a). Degradome sequencing reveals endogenous small RNA targets in rice (Oryza sativa L. ssp.indica). Frontiers in Biology, 5, 67–90.

    Article  CAS  Google Scholar 

  • Zhou, M., Li, D., Li, Z., Hu, Q., Yang, C., Zhu, L., et al. (2013). Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiology, 161, 1375–1391.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, L., Liu, Y., Liu, Z., Kong, D., Duan, M., & Luo, L. (2010b). Genome wide identification and analysis of drought-responsive microRNAs in Oryza sativa. Journal of Experimental Botany, 61, 4157–4168.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, Z. S., Song, J. B., & Yang, Z. M. (2012a). Genome-wide identification of Brassica napus microRNAs and their targets reveals their differential regulation by cadmium. Journal of Experimental Botany, 59, 3443–3452.

    Google Scholar 

  • Zhou, Z. S., Zeng, H. Q., Liu, Z. P., & Yang, Z. M. (2012b). Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant Cell Environment, 35, 86–99.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zou, Y., Wang, Y., Wang, L., Yang, L., Wang, R., & Li, X. (2013). miR172b controls the transition to autotrophic development inhibited by ABA in Arabidopsis. PLoS One, 8, e64770.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

SKM is highly thankful to the Director, IIRR, for his kind support. Financial support received from DBT Grant (BT/PR6466/COE/34/16/2012) is acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Satendra K. Mangrauthia.

Additional information

Satendra K. Mangrauthia and A. Maliha contributed equally.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mangrauthia, S.K., Maliha, A., Prathi, N.B. et al. MicroRNAs: potential target for genome editing in plants for traits improvement. Ind J Plant Physiol. 22, 530–548 (2017). https://doi.org/10.1007/s40502-017-0326-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40502-017-0326-8

Keywords

Navigation