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Characterization and expression pattern analysis of microRNAs in wheat under drought stress

  • Original Papers
  • Published:
Biologia Plantarum

Abstract

Plant microRNAs (miRNAs) play important roles in regulating plant growth, development, and responses to abiotic stresses. In this study, 38 miRNAs (TaMIRs) from wheat (Triticum aestivum L.), 36 from the miRBase database, and two from our previous work were characterized and subjected to an expression pattern analysis under normal conditions and a drought stress. A semiquantitative reverse transcriptase polymerase chain reaction (RT-PCR), real-time quantitative PCR (qPCR), and small RNA blot analyses revealed that two TaMIRs (TaMIR1120 and TaMIR1123) were root-predominant and two TaMIRs (TaMIR1121 and TaMIR1134) were leaf-predominant. Seven TaMIR precursors showed altered expressions after the drought; of these, TaMIR1136 was upregulated, whereas TaMIR156, TaMIR408, TaMIR1119, TaMIR1129, TaMIR1133, and TaMIR1139 were downregulated. These seven drought-responsive TaMIRs showed dose-dependent and typical temporal expression patterns during drought induction, and they gradually returned back under the normal growth conditions. The drought-responsive and the tissue-predominant TaMIRs had varying numbers of target genes. Randomly selected target genes exhibited opposite expression patterns to their corresponding TaMIRs suggesting that they were regulated by distinct TaMIRs through a post-transcriptional cleavage. The target genes regulated by drought-responsive and tissue-predominant TaMIRs are involved in various cellular processes, such as signal transduction, transcriptional regulation, primary and secondary metabolisms, development, and defense responses. These results provide a novel insight into the miRNA-mediated responses of wheat to drought stress.

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Abbreviations

ABA:

abscisic acid

AFB3 :

auxin receptor 3 gene

CSD :

cytosolic Cu/Zn superoxide dismutase genes

DRE:

dehydration-responsive element

EST:

expressed sequence tag

MS:

Murashige and Skoog

PEG:

polyethylene glycol

Pi:

inorganic phosphate

qPCR:

real-time quantitative PCR

RISC:

RNA-induced silencing complex

RT-PCR:

reverse transcriptase polymerase chain reaction

TaMIR:

Triticum aestivum microRNA

References

  • Allen, E., Xie, Z., Gustafson, A.M., Carrington, J.C.: MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. — Cell 121: 207–221, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Almeida, T., Pinto, G., Correia, B., Santos, C., Gonçalves, S.: QsMYB1 expression is modulated in response to heat and drought stresses and during plant recovery in Quercus suber. — Plant Physiol. Biochem. 73: 274–281, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Barrera-Figueroa, B.E., Gao, L., Diop, N.N., Wu, Z., Ehlers, J.D., Roberts, P.A., Close, T.J., Zhu, J.K., Liu, R.: Identification and comparative analysis of drought-associated microRNAs in two cowpea genotypes. — PLoS One 7: e30039, 2012.

    Article  Google Scholar 

  • Bartel, D.P.: MicroRNAs: genomics, biogenesis, mechanism, and function. — Cell 116: 281–297, 2010.

    Article  Google Scholar 

  • Bruex, A., Kainkaryam, R.M., Wieckowski, Y., Kang, Y.H., Bernhardt, C., Xia, Y., Zheng, X., Wang, J.Y., Lee, M.M., Benfey, P., Woolf, P.J., Schiefelbein, J.: A gene regulatory network for root epidermis cell differentiation in Arabidopsis. — PLoS Genet. 8: e1002446, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Choi, H.W., Hwang, B.K.: The pepper extracellular peroxidase CaPO2 is required for salt, drought and oxidative stress tolerance as well as resistance to fungal pathogens. — Planta 235: 1369–1382, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Dalmay, T.: Mechanism of miRNA-mediated repression of mRNA translation. — Essays Biochem. 54: 29–38, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Ferreira, T.H., Gentile, A., Vilela, R.D., Costa, G.G.L., Dias, L.I., Endres, L., Menossi, M.: microRNAs associated with drought response in the bioenergy crop sugarcane (Saccharum spp.). — BMC Plant Biol. 11: 127, 2011.

    Article  Google Scholar 

  • Fleury, D., Jefferies, S., Kuchel, H., Langridge, P.: Genetic and genomic tools to improve drought tolerance in wheat. — J. exp. Bot. 61: 3211–3222, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Gómez-Porras, J.L., Riaño-Pachón, D.M., Dreyer, I., Mayer, J.E., Mueller-Roeber, B.: Genome-wide analysis of ABA-responsive elements ABRE and CE3 reveals divergent patterns in Arabidopsis and rice. — BMC Genom. 8: 260, 2007.

    Article  Google Scholar 

  • Kang, G.Z., Li, G. Z., Liu, G.Q., Wu, W., Peng, X.Q., Wang, C.Y., Zhu, Y.J., Guo, T.C.: Exogenous salicylic acid enhances wheat drought tolerance by influence on the expression of genes related to ascorbate-glutathione cycle. — Biol. Plant. 57: 718–724, 2013.

    Article  CAS  Google Scholar 

  • Kayihan, C., Eyidogan, F., Afsar, N., Oktem, H.A., Yucel, M.: Cu/Zn superoxide dismutase activity and respective gene expression during cold acclimation and freezing stress in barley cultivars. — Biol. Plant. 56: 693–698, 2012.

    Article  CAS  Google Scholar 

  • Kong, Y., Elling, A.A., Chen, B., Deng, X.W.: Differential expression of microRNAs in maize inbred and hybrid lines during salt and drought stress. — Amer. J. Plant Sci. 1: 69–76, 2010.

    Article  CAS  Google Scholar 

  • Kantar, M., Lucas, S.J., Budak, H.: miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. — Planta 233: 471–484, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Li, J., Guo, G., Guo, W., Guo, G., Tong, D., Ni, Z., Sun, Q., Yao, Y.: miRNA164-directed cleavage of ZmNAC1 confers lateral root development in maize (Zea mays L.). — BMC Plant Biol. 12: 220, 2012a.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li, W., Cui, X., Meng, Z., Huang, X., Xie, Q., Wu, H., Jin, H., Zhang, D., Liang, W.: Transcriptional regulation of Arabidopsis MIR168a and ARGONAUTE1 homeostasis in abscisic acid and abiotic stress responses. — Plant Physiol. 158: 1279–1292, 2012b.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the \(2^{ - \Delta \Delta C_T }\) method. — Methods 25: 402–408, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Maruyama, K., Todaka, D., Mizoi, J., Yoshida, T., Kidokoro, S., Matsukura, S., Takasaki, H., Sakurai, T., Yamamoto, Y.Y., Yoshiwara, K., Kojima, M., Sakakibara, H., Shinozaki, K., Yamaguchi-Shinozaki, K.: Identification of cis-acting promoter elements in cold- and dehydration-induced transcriptional pathways in Arabidopsis, rice, and soybean. — DNA Res. 19: 37–49, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Millar, A.A., Waterhouse, P.M.: Plant and animal microRNAs: similarities and differences. — Funct. Integr. Genom. 5: 129–135, 2005.

    Article  CAS  Google Scholar 

  • Movahedi, S., Sayed Tabatabaei, B.E., Alizade, H., Ghobadi, C.: Constitutive expression of Arabidopsis DREB1B in transgenic potato enhances drought and freezing tolerance. — Biol. Plant. 56: 37–42, 2012.

    Article  CAS  Google Scholar 

  • Mutum, R.D., Balyan, S.C., Kansal, S., Agarwal, P., Kumar, S., Kumar, M., Raghuvanshi, S.: Evolution of variety-specific regulatory schema for expression of osa-miR408 in indica rice varieties under drought stress. — FEBS J. 280: 1717–1730, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Ram, G., Sharma, A.D.: In silico analysis of putative miRNAs and their target genes in sorghum (Sorghum bicolor). — Int. J. Bioinform. Res. Appl. 9: 233, 2013.

    Article  Google Scholar 

  • Seo, P.J., Xiang, F., Qiao, M., Park, J.Y., Lee, Y.N., Kim, S.G., Lee, Y.H., Park, W.J., Park, C.M.: The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. — Plant Physiol. 151: 275–289, 2009.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shinozaki, K., Yamaguchi-Shinozaki, K.: Gene expression and signal transduction in water-stress response. — Plant Physiol. 115: 327–334, 1997.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shuai, P., Liang, D., Zhang, Z., Yin, W., Xia, X.: Identification of drought-responsive and novel Populus trichocarpa microRNAs by high-throughput sequencing and their targets using degradome analysis. — BMC Genom. 14: 233, 2013.

    Article  CAS  Google Scholar 

  • Song, J.B., Gao, S., Sun, D., Li, H., Shu, X.X., Yang, Z.M.: miR394 and LCR are involved in Arabidopsis salt and drought stress responses in an abscisic acid-dependent manner. — BMC Plant Biol. 13: 210, 2013.

    Article  PubMed Central  PubMed  Google Scholar 

  • Sun, Z.H., Ding, C.H, Li, X.M, Xiao, K.: Molecular characterization and expression analysis of TaZFP15, a C2H2- type zinc finger transcription factor gene in wheat (Triticum aestivum L.). — J. integr. Agr. 11: 31–42, 2012.

    Article  CAS  Google Scholar 

  • Sunkar, R.: MicroRNAs with macro-effects on plant stress responses. — Semin. Cell Dev. Biol. 21: 805–811, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Sunkar, R., Kapoor, A., Zhu, J.K.: 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, 2006.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tang, Z., Zhang, L., Xu, C., Yuan., S., Zhang, F., Zheng, Y., Zhao, C.: Uncovering small RNA-mediated responses to cold stress in a wheat thermosensitive genic male-sterile line by deep sequencing. — Plant Physiol. 159: 721–738, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tian, F.X., Gong, J.F., Wang, G.P., Wang, G.K., Fan, Z.Y., Wang, W.: Improved drought resistance in a wheat stay-green mutant tasg1 under field conditions. — Biol. Plant. 56: 509–515, 2012.

    Article  Google Scholar 

  • Toker, C., Canci, H., Yildirim, T.: Evaluation of perennial wild Cicer species for drought resistance. — Genet. Resour. Crop Evol. 54: 1781–1786, 2007.

    Article  Google Scholar 

  • Umezawa, T., Nakashima, K., Miyakawa, T., Kuromori, T., Tanokura, M., Shinozaki, K., Yamaguchi-Shinozaki, K.: Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. — Plant Cell Physiol. 51: 1821–1839, 2010.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vidal, E.A., Araus, V., Lu, C., Parry, G., Green, P.J., Coruzzi, G.M., Gutiérrez, R.A.: Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. — Proc. nat. Acad. Sci. USA 9: 349–364, 2013.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Vivek, P.J., Tuteja, N., Soniya, E.V.: CDPK1 from ginger promotes salinity and drought stress tolerance without yield penalty by improving growth and photosynthesis in Nicotiana tabacum. — PLoS One 23: e76392, 2013.

  • Won, S.K., Lee, Y., Lee, H.Y., Heo, Y.K., Cho, M., Cho, H.T.: cis-element- and transcriptome-based screening of root hair-specific genes and their functional characterization in Arabidopsis. — Plant Physiol. 150: 1459–1473, 2009.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xia, K., Wang, R., Qu, X., Fang, Z., Tian, C., Duan, J., Wang, Y., Zhang, M.: OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. — Proc. nat. Acad. Sci. USA 107: 4477–4482, 2010.

    Article  Google Scholar 

  • Xin, M., Wang, Y., Yao., Y, Xie, C., Peng, H., Ni, Z., Sun, Q.: Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). — BMC Plant Biol. 10: 123, 2010.

    Article  PubMed Central  PubMed  Google Scholar 

  • Xu, W., Yang, R., Li, M., Xing, Z., Chen, G., Guo, H., Gong, X., Du, Z., Zhang, Z., Hu X., Wang D., Qian, Q., Wang, T., Su, Z., Xue, Y.: Transcriptome phase distribution analysis reveals diurnal regulated biological processes and key pathways in rice flag leaves and seedling leaves. — PLoS One 6: e17613, 2011a.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xu, Z., Zhong, S., Li, X., Li, W., Rothstein, SJ, Zhang, S, Bi, Y, Xie, C.: Genome-wide identification of microRNAs in response to low nitrate availability in maize leaves and roots. — PLoS One 6: e28009, 2011b.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang, L., Wu, G., Poethig, R.S.: Mutations in the GW-repeat protein SUO reveal a developmental function for microRNA-mediated translational repression in Arabidopsis. — Proc. nat. Acad. Sci. USA 109: 315–320, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang, H.M., Zhang, L.S., Liu, L., Zhu, W.N., Yang, W.B.: Changes of dehydrin profiles induced by drought in winter wheat at different developmental stages. — Biol. Plant. 57: 797–800, 2013.

    Article  CAS  Google Scholar 

  • Zhang, L., Yu, S., Zuo, K., Luo, L., Tang, K.: Identification of gene modules associated with drought response in rice by network-based analysis. — PLoS One 7: e33748, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang, L., Xie, X., Song, Y., Jiang, F., Zhu, C., Wen, F.: Viral resistance mediated by shRNA depends on the sequence similarity and mismatched sites between the target sequence and siRNA. — Biol. Plant. 57: 547–554, 2013.

    Article  CAS  Google Scholar 

  • Zhang, Z., Wei, L., Zou, X., Tao, Y., Liu, Z., Zheng, Y.: Submergence-responsive MicroRNAs are potentially involved in the regulation of morphological and metabolic adaptations in maize root cells. — Ann Bot. 102: 509–519, 2008.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao, X., Liu, X., Guo, C., Gu, J., Xiao, K.: Identification and characterization of microRNAs from wheat (Triticum aestivum L.) under phosphorus deprivation. — J. Plant Biochem. Biotechnol. 22: 113–123, 2013.

    Article  CAS  Google Scholar 

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Correspondence to K. Xiao.

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Acknowledgments: We would like to thank two anonymous reviewers and the editors whose detailed comments and careful work helped to improve the manuscript. This work was financially supported by the National Science Foundation of China (No. 31371618, 31201674), the Natural Science Foundation of Hebei (C2013204094) and the Key Laboratory of Crop Growth Regulation of Hebei Province.

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Zhao, Y.Y., Guo, C.J., Li, X.J. et al. Characterization and expression pattern analysis of microRNAs in wheat under drought stress. Biol Plant 59, 37–46 (2015). https://doi.org/10.1007/s10535-014-0463-0

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  • DOI: https://doi.org/10.1007/s10535-014-0463-0

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