Abstract
MicroRNAs (miRNAs) are a class of small non-coding regulatory RNAs that regulate gene expression by guiding target mRNA cleavage or translational inhibition. Drought is a common environmental stress influencing crop growth and development. To date, it has been reported that a number of plant miRNA are involved in drought stress response. In this study, we comparatively investigated drought stress-responsive miRNAs in the root and leaf of bread wheat (Triticum aestivum cv. Sivas 111/33) by miRNA microarray screening. miRNA microarray analysis showed that 285 miRNAs (207 upregulated and 78 downregulated) and 244 miRNAs (115 upregulated and 129 downregulated) were differentially expressed in leaf and root tissues, respectively. Among the differentially expressed miRNAs, 23 miRNAs were only expressed in the leaf and 26 miRNAs were only expressed in the root of wheat growth under drought stress. Upon drought treatment, expression of miR159, miR160, miR166, miR169, miR172, miR395, miR396, miR408, miR472, miR477, miR482, miR1858, miR2118, and miR5049 were found to be significantly differentiated in bread wheat. The regulatory network analysis showed that miR395 has connections with a number of target transcripts, and miR159 and miR319 share a number of target genes. Drought-tolerant and drought-sensitive wheat cultivars showed altered expression pattern upon drought stress in terms of investigated miRNA and their target transcript expression level.
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References
Barrera-Figueroa BE, Gao L, Diop NN, Wu Z, Ehlers JD, Roberts PA, Close TJ, Zhu JK, Liu R (2011) Identification and comparative analysis of drought-associated microRNAs in two cowpea genotypes. BMC Plant Biol 11:127. doi:10.1186/1471-2229-11-127
Boke H, Ozhuner E, Turktas M, Parmaksiz I, Ozcan S, Unver T (2015) Regulation of the alkaloid biosynthesis by miRNA in opium poppy. Plant Biotechnol J 13:409–420. doi:10.1111/pbi.12346
Boualem A, Laporte P, Jovanovic M, Laffont C, Plet J, Combier JP, Niebel A, Crespi M, Frugier F (2008) MicroRNA166 controls root and nodule development in Medicago truncatula. Plant J: Cell Mol Biol 54:876–887. doi:10.1111/j.1365-313X.2008.03448.x
Casella G, Berger RL (2002) Statistical Inference, 2. Duxbury Pacific Grove, CA
Clark JI, Brooksbank C, Lomax J (2005) It’s all GO for plant scientists. Plant Physiol 138:1268–1279. doi:10.1104/pp. 104.058529
Cleveland WS (1979) Robust locally weighted regression and smoothing scatterplots. J Am Stat Assoc 74
Ding Y, Tao Y, Zhu C (2013) Emerging roles of microRNAs in the mediation of drought stress response in plants. J Exp Bot 64:3077–3086. doi:10.1093/jxb/ert164
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70. doi:10.1093/nar/gkq310
Eldem V, Celikkol Akcay U, Ozhuner E, Bakir Y, Uranbey S, Unver T (2012) Genome-wide identification of miRNAs responsive to drought in peach (Prunus persica) by high-throughput deep sequencing. PLoS One 7, e50298. doi:10.1371/journal.pone.0050298
Eldem V, Okay S, Unver T (2013) Plant microRNAs: new players in functional genomics. Turk J Agric For 37:1–21
Eren H, Pekmezci MY, Okay S, Turktas M, Inal B, Ilhan E, Atak M, Erayman M, Unver T (2015) Hexaploid wheat (Triticum aestivum) root miRNome analysis in response to salt stress. Ann Appl Biol. doi:10.1111/aab.12219
Frazier T, Sun G, Burklew C, Zhang B (2011) Salt and drought stresses induce the aberrant expression of microRNA genes in tobacco. Mol Biotechnol 49:159–165. doi:10.1007/s12033-011-9387-5
Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043. doi:10.1016/j.cub.2005.10.016
Gupta OP, Meena NL, Sharma I, Sharma P (2014) Differential regulation of microRNAs in response to osmotic, salt and cold stresses in wheat. Mol Biol Rep 41:4623–4629. doi:10.1007/s11033-014-3333-0
Hajyzadeh M, Turktas M, Khawar KM, Unver T (2015) miR408 overexpression causes increased drought tolerance in chickpea. Gene 555:186–193. doi:10.1016/j.gene.2014.11.002
Inal B, Turktas M, Eren H, Ilhan E, Okay S, Atak M, Erayman M, Unver T (2014) Genome-wide fungal stress responsive miRNA expression in wheat. Planta 240:1287–1298. doi:10.1007/s00425-014-2153-8
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799. doi:10.1016/j.molcel.2004.05.027
Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53. doi:10.1146/annurev.arplant.57.032905.105218
Kantar M, Unver T, Budak H (2010) Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Funct Integr Genom 10:493–507. doi:10.1007/s10142-010-0181-4
Kantar M, Lucas SJ, Budak H (2011) miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233:471–484. doi:10.1007/s00425-010-1309-4
Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819:137–148. doi:10.1016/j.bbagrm.2011.05.001
Kumimoto RW, Adam L, Hymus GJ, Repetti PP, Reuber TL, Marion CM, Hempel FD, Ratcliffe OJ (2008) The Nuclear Factor Y subunits NF-YB2 and NF-YB3 play additive roles in the promotion of flowering by inductive long-day photoperiods in Arabidopsis. Planta 228:709–723. doi:10.1007/s00425-008-0773-6
Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20:2238–2251. doi:10.1105/tpc.108.059444
Li Y, Li C, Ding G, Jin Y (2011) Evolution of MIR159/319 microRNA genes and their post-transcriptional regulatory link to siRNA pathways. BMC Evol Biol 11:122. doi:10.1186/1471-2148-11-122
Li J-S, Fu F-L, An M, Zhou S-F, She Y-H, Li W-C (2013) Differential expression of microRNAs in response to drought stress in maize. J Integr Agric 12:1414–1422. doi:10.1016/S2095-3119(13)60311-1
Li C, Ng CKY, Fan L-M (2015) MYB transcription factors, active players in abiotic stress signaling. Environ Exp Bot 114:80–91. doi:10.1016/j.envexpbot.2014.06.014
Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14:836–843. doi:10.1261/rna.895308
Liu D, Song Y, Chen Z, Yu D (2009) Ectopic expression of miR396 suppresses GRF target gene expression and alters leaf growth in Arabidopsis. Physiol Plant 136:223–236. doi:10.1111/j.1399-3054.2009.01229.x
Lu XY, Huang XL (2008) Plant miRNAs and abiotic stress responses. Biochem Biophys Res Commun 368:458–462. doi:10.1016/j.bbrc.2008.02.007
Lu S, Sun Y-H, Shi R, Clark C, Li L, Chiang VL (2005) Novel and mechanical stress–responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17:2186–2203
Miura K, Furumoto T (2013) Cold signaling and cold response in plants. Int J Mol Sci 14:5312–5337. doi:10.3390/ijms14035312
Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185. doi:10.1093/nar/gkm321
Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439. doi:10.1126/science.1126088
Pandey B, Gupta OP, Pandey DM, Sharma I, Sharma P (2013) Identification of new stress-induced microRNA and their targets in wheat using computational approach. Plant Signal Behav 8, e23932. doi:10.4161/psb.23932
Pandey R, Joshi G, Bhardwaj AR, Agarwal M, Katiyar-Agarwal S (2014) A comprehensive genome-wide study on tissue-specific and abiotic stress-specific miRNAs in Triticum aestivum. PLoS One 9, e95800. doi:10.1371/journal.pone.0095800
Reyes JL, Chua NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J: Cell Mol Biol 49:592–606. doi:10.1111/j.1365-313X.2006.02980.x
Shanker AK, Maheswari M, Yadav SK, Desai S, Bhanu D, Attal NB, Venkateswarlu B (2014) Drought stress responses in crops. Funct Integr Genom 14:11–22. doi:10.1007/s10142-013-0356-x
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. doi:10.1101/gr.1239303
Shiriga K, Sharma R, Kumar K, Yadav SK, Hossain F, Thirunavukkarasu N (2014) Genome-wide identification and expression pattern of drought-responsive members of the NAC family in maize. Meta Gene 2:407–417. doi:10.1016/j.mgene.2014.05.001
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019. doi:10.1105/tpc.104.022830
Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:301–309. doi:10.1016/j.tplants.2007.05.001
Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu JK (2008) Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 8:25. doi:10.1186/1471-2229-8-25
Sunkar R, Li YF, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203. doi:10.1016/j.tplants.2012.01.010
Trindade I, Capitao C, Dalmay T, Fevereiro MP, Santos DM (2010) miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula. Planta 231:705–716. doi:10.1007/s00425-009-1078-0
Unver T, Namuth-Covert DM, Budak H (2009) Review of current methodological approaches for characterizing microRNAs in plants. Int J Plant Genomics 2009:262463. doi:10.1155/2009/262463
Unver T, Bakar M, Shearman RC, Budak H (2010) Genome-wide profiling and analysis of Festuca arundinacea miRNAs and transcriptomes in response to foliar glyphosate application. Mol Gen Genomics 283:397–413. doi:10.1007/s00438-010-0526-7
Van Bel M, Proost S, Van Neste C, Deforce D, Van de Peer Y, Vandepoele K (2013) TRAPID: an efficient online tool for the functional and comparative analysis of de novo RNA-Seq transcriptomes. Genome Biol 14:R134. doi:10.1186/gb-2013-14-12-r134
Wang T, Chen L, Zhao M, Tian Q, Zhang WH (2011) Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 12:367. doi:10.1186/1471-2164-12-367
Wang B, Sun YF, Song N, Wang XJ, Feng H, Huang LL, Kang ZS (2013) Identification of UV-B-induced microRNAs in wheat. Genet Mol Res 12:4213–4221. doi:10.4238/2013.October.7.7
Wu S, Hu C, Tan Q, Nie Z, Sun X (2014) Effects of molybdenum on water utilization, antioxidative defense system and osmotic-adjustment ability in winter wheat (Triticum aestivum) under drought stress. Plant Physiol Biochem: Soc Fr Physiol Veg 83:365–374. doi:10.1016/j.plaphy.2014.08.022
Xin M, Wang Y, Yao Y, Xie C, Peng H, Ni Z, Sun Q (2010) Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biol 10:123. doi:10.1186/1471-2229-10-123
Yang F-X, Yu D-Q (2010) Overexpression of Arabidopsis MiR396 enhances drought tolerance in transgenic tobacco plants: overexpression of Arabidopsis MiR396 enhances drought tolerance in transgenic tobacco plants. Acta Bot Yunnanica 31:421–426. doi:10.3724/SP.J.1143.2010.00421
Zhang B (2015) MicroRNA: a new target for improving plant tolerance to abiotic stress. J Exp Bot 66:1749–1761. doi:10.1093/jxb/erv013
Zhang X, Zou Z, Gong P, Zhang J, Ziaf K, Li H, Xiao F, Ye Z (2011) Over-expression of microRNA169 confers enhanced drought tolerance to tomato. Biotechnol Lett 33:403–409. doi:10.1007/s10529-010-0436-0
Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, Ruan K, Jin Y (2007) Identification of drought-induced microRNAs in rice. Biochem Biophys Res Commun 354:585–590. doi:10.1016/j.bbrc.2007.01.022
Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61:4157–4168. doi:10.1093/jxb/erq237
Zhou M, Li D, Li Z, Hu Q, Yang C, Zhu L, Luo H (2013) Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiol 161:1375–1391. doi:10.1104/pp. 112.208702
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The study is partly supported by TUBITAK with grant number 113O016. Dr. Yasin F. Dagdas of The Sainsbury Laboratory, Norwich, UK, kindly proofread the manuscript.
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Akdogan, G., Tufekci, E.D., Uranbey, S. et al. miRNA-based drought regulation in wheat. Funct Integr Genomics 16, 221–233 (2016). https://doi.org/10.1007/s10142-015-0452-1
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DOI: https://doi.org/10.1007/s10142-015-0452-1