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Dehydration-responsive miRNAs in foxtail millet: genome-wide identification, characterization and expression profiling

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Abstract

Main Conclusion

A set of novel and known dehydration-responsive miRNAs have been identified in foxtail millet. These findings provide new insights into understanding the functional role of miRNAs and their respective targets in regulating plant response to dehydration stress.

MicroRNAs perform significant regulatory roles in growth, development and stress response of plants. Though the miRNA-mediated gene regulatory networks under dehydration stress remain largely unexplored in plant including foxtail millet (Setaria italica), which is a natural abiotic stress tolerant crop. To find out the dehydration-responsive miRNAs at the global level, four small RNA libraries were constructed from control and dehydration stress treated seedlings of two foxtail millet cultivars showing contrasting tolerance behavior towards dehydration stress. Using Illumina sequencing technology, 55 known and 136 novel miRNAs were identified, representing 22 and 48 miRNA families, respectively. Eighteen known and 33 novel miRNAs were differentially expressed during dehydration stress. After the stress treatment, 32 dehydration-responsive miRNAs were up-regulated in tolerant cultivar and 22 miRNAs were down-regulated in sensitive cultivar, suggesting that miRNA-mediated molecular regulation might play important roles in providing contrasting characteristics to these cultivars. Predicted targets of identified miRNAs were found to encode various transcription factors and functional enzymes, indicating their involvement in broad spectrum regulatory functions and biological processes. Further, differential expression patterns of seven known miRNAs were validated by northern blot and expression of ten novel dehydration-responsive miRNAs were confirmed by SL-qRT PCR. Differential expression behavior of five miRNA-target genes was verified under dehydration stress treatment and two of them also validated by RLM RACE. Overall, the present study highlights the importance of dehydration stress-associated post-transcriptional regulation governed by miRNAs and their targets in a naturally stress-tolerant model crop.

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Abbreviations

GRF:

Growth regulating factor

MFE:

Minimum fold energy

miRNA*:

MicroRNA star

RLM-5′ Race:

RNA ligase mediated 5′ rapid amplification of cDNA ends

RPM:

Reads per million

SBP:

Squamosa promoter-binding protein

SL-qRT:

Stem loop quantitative real time PCR

References

  • Ahuja I, de Vos RCH, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15:664–674

    Article  PubMed  CAS  Google Scholar 

  • Allen E, Xie Z, Gustafson A, Sung G, Spatafora J, Carrington J (2004) Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat Genet 36:1282–1290

    Article  PubMed  CAS  Google Scholar 

  • Baldwin L, Domon JM, Klimek JF, Fournet F, Sellier H, Gillet F, Pelloux J, Lejeune-Hénaut I, Carpita NC, Rayon C (2014) Structural alteration of cell wall pectins accompanies pea development in response to cold. Phytochemistry 104:37–47

    Article  PubMed  CAS  Google Scholar 

  • Barakat A, Sriram A, Park J, Zhebentyayeva T, Main D, Abbott A (2012) Genome wide identification of chilling responsive microRNAs in Prunus persica. BMC Genom 13:1–11

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bennetzen J, Schmutz J, Wang H et al (2012) Reference genome sequence of the model plant Setaria. Nat Biotechnol 30:555–561

    Article  PubMed  CAS  Google Scholar 

  • Bologna N, Schapire A, Palatnik J (2013) Processing of plant microRNA precursors. Brief Funct Genomics 12:37–45

    Article  PubMed  CAS  Google Scholar 

  • Boualem A, Laporte P, Jovanovic M, Laffont C, Plet J, Combier J-P, Niebel A, Crespi M, Frugier F (2008) MicroRNA166 controls root and nodule development in Medicago truncatula. Plant J 54:876–887

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cheah BH, Nadarajah K, Divate MD, Wickneswari R (2015) Identification of four functionally important microRNA families with contrasting differential expression profiles between drought-tolerant and susceptible rice leaf at vegetative stage. BMC Genom 16:692

    Article  Google Scholar 

  • Chen X (2005) microRNA biogenesis and function in plants. FEBS Lett 579:5923–5931

    Article  PubMed  CAS  Google Scholar 

  • Chen X (2009) Small RNAs and their roles in plant development. Annu Rev Cell Devel Biol 25:21–44

    Article  CAS  Google Scholar 

  • Chen C, Ridzon D, Broomer A, Zhou Z, Lee D, Nguyen J, Barbisin M, Xu N, Mahuvakar V, Andersen M (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33:e179

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Chen L, Ren Y, Zhang Y, Xu J, Sun F, Zhang Z, Wang Y (2012a) Genome-wide identification and expression analysis of heat-responsive and novel microRNAs in Populus tomentosa. Gene 504:160–165

    Article  PubMed  CAS  Google Scholar 

  • Chen L, Wang T, Zhao M, Tian Q, Zhang W (2012b) Identification of aluminum-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. Planta 235:375–386

    Article  PubMed  CAS  Google Scholar 

  • Colaiacovo M, Subacchi A, Bagnaresi P, Lamontanara A, Cattivelli L, Facciol P (2010) A computational-based update on microRNAs and their targets in barley (Hordeum vulgare L.). BMC Genom 11:595

    Article  CAS  Google Scholar 

  • Cuperus JT, Fahlgren N, Carrington JC (2011) Evolution and functional diversification of MIRNA genes. Plant Cell 23:431–442

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Diao X (2007) Foxtail millet production and future development direction in China. In: Chai Y, Wan SH (eds) Reports on minor grain development in China. Chinese Agri Sci Tech Press, Beijing, pp 32–43

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Fahlgren N, Howell M, Kasschau K, Chapman E, Sullivan C, Cumbie J, Givan S, Law T, Grant S, Dangl J (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2:e219

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fang Y, Xie K, Xiong L (2014) Conserved miR164-targeted NAC genes negatively regulate drought resistance in rice. J Exp Bot 65:2119–2135

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fujii H, Chiou T, Lin S, Aung K, Zhu J (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2204. doi:10.1016/j.cub.2005.10.016

    Article  PubMed  CAS  Google Scholar 

  • Gao Z, Shi T, Luo X, Zhang Z, Zhuang W, Wang L (2012) High-throughput sequencing of small RNAs and analysis of differentially expressed microRNAs associated with pistil development in Japanese apricot. BMC Genom 13:371

    Article  CAS  Google Scholar 

  • Gentile A, Dias LI, Mattos RS, Ferreira TH, Menossi M (2015) MicroRNAs and drought responses in sugarcane. Front Plant Sci 6:58

    Article  PubMed Central  PubMed  Google Scholar 

  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gu Y, Liu Y, Zhang J, Liu H, Hu Y, Du H, Li Y, Chen J, Wei B, Huang Y (2013) Identification and characterization of microRNAs in the developing maize endosperm. Genomics 102:472–478

    Article  PubMed  CAS  Google Scholar 

  • Han J, Xie H, Sun Q, Wang J, Lu M, Wang W, Guo E, Pan J (2014) Bioinformatic identification and experimental validation of miRNAs from foxtail millet (Setaria italica). Gene 546:367–377

    Article  PubMed  CAS  Google Scholar 

  • Hawker NP, Bowman JL (2004) Roles for Class III HD-Zip and KANADI genes in Arabidopsis root development. Plant Physiol 135:2261–2270

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hofacker IL, Fontana W, Stadler PF, Bonhoeffer LS, Tacker M, Schuster P (1994) Fast folding and comparison of RNA secondary structures. Monatsh Chem 125:167–188

    Article  CAS  Google Scholar 

  • Hsieh L-C, Lin S-I, Shih AC-C, Chen J-W, Lin W-Y, Tseng C-Y, Li W-H, Chiou T-J (2009) Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151:2120–2132

    Article  PubMed Central  PubMed  Google Scholar 

  • Jeong D-H, Park S, Zhai J, Gurazada SGR, De Paoli E, Meyers BC, Green PJ (2011) Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23:4185–4207

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jia G, Huang X, Zhi H et al (2013) A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtail millet (Setaria italica). Nature Genet 45:957–961

    Article  PubMed  CAS  Google Scholar 

  • Jones-Rhoades M, Bartel D, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    Article  PubMed  CAS  Google Scholar 

  • Khan Y, Yadav A, Bonthala VS, Muthamilarasan M, Yadav CB, Prasad M (2014) Comprehensive genome-wide identification and expression profiling of foxtail millet [Setaria italica (L.)] miRNAs in response to abiotic stress and development of miRNA database. Plant Cell Tiss Organ Cult 118:279–292

    Article  CAS  Google Scholar 

  • Khraiwesh B, Zhu J-K, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819:137–148

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kole C, Muthamilarasan M, Henry R, Edwards D, Sharma R, Abberton M, Batley J, Bentley A, Blakeney M, Bryant J, Cai H et al (2015) Application of genomics-assisted breeding for generation of climate resilient crops: progress and prospects. Front Plant Sci 6:563

    Article  PubMed Central  PubMed  Google Scholar 

  • Kubacka-Zebalska M, Kacperska A (1999) Low temperature-induced modifications of cell wall content and polysaccharide composition in leaves of winter oilseed rape (Brassica napus L. var. oleifera L.). Plant Sci 148:59–67

    Article  CAS  Google Scholar 

  • Kumar K, Muthamilarasan M, Prasad M (2013) Reference genes for quantitative real-time PCR analysis in the model plant foxtail millet (Setaria italica L.) subjected to abiotic stress conditions. Plant Cell Tissue Organ Cult 115:13–22

    Article  CAS  Google Scholar 

  • Lata C, Bhutty S, Bahadur RP, Majee M, Prasad M (2011) Association of an SNP in a novel DREB2-like gene SiDREB2 with stress tolerance in foxtail millet [Setaria italica (L.)]. J Exp Bot 62:3387–3401

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lata C, Gupta S, Prasad M (2013) Foxtail millet: a model crop for genetic and genomic studies in bioenergy grasses. Crit Rev Biotechnol 33:328–343

    Article  PubMed  Google Scholar 

  • Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lelandais-Briere C, Naya L, Sallet E, Calenge F, Frugier F, Hartmann C, Gouzy J, Crespi M (2009) Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell 21:2780–2796

    Article  PubMed Central  PubMed  Google Scholar 

  • Li B, Qin Y, Duan H, Yin W, Xia X (2011) Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J Exp Bot 62:3765–3779

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Li B, Duan H, Li J, Deng X, Yin W, Xia X (2013) Global identification of miRNAs and targets in Populus euphratica under salt stress. Plant Mol Biol 81:525–539

    Article  PubMed  CAS  Google Scholar 

  • Liang G, Yang F, Yu D (2010) MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J 62:1046–1057

    PubMed  CAS  Google Scholar 

  • Lin Y, Lai Z (2013) Comparative analysis reveals dynamic changes in miRNAs and their targets and expression during somatic embryogenesis in longan (Dimocarpus longan Lour.). PLoS One 8:e60337

    Article  PubMed Central  PubMed  CAS  Google Scholar 

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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2∆(-Delta Delta CT) method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Lu C, Meyers BC, Green PJ (2007) Construction of small RNA cDNA libraries for deep sequencing. Methods 43:110–117

    Article  PubMed  CAS  Google Scholar 

  • Macovei A, Gill SS, Tuteja N (2012) microRNAs as promising tools for improving stress tolerance in rice. Plant Signal Behav 7:1296–1301

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28:67–77

    Article  PubMed  CAS  Google Scholar 

  • Martinez G, Forment J, Llave C, Pallas V, Gomez G (2011) High-throughput sequencing, characterization and detection of new and conserved cucumber miRNAs. PLoS One 6:e19523

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • McCormack JE, Hird SM, Zellmer AJ, Carstens BC, Brumfield RT (2013) Applications of next-generation sequencing to phylogeography and phylogenetics. Mol Phylogenet Evol 66:526–538

    Article  PubMed  CAS  Google Scholar 

  • Meyers B, Axtell M, Bartel B, Bartel D, Baulcombe D, Bowman J, Cao X, Carrington J, Chen X, Green P (2008) Criteria for annotation of plant microRNAs. Plant Cell 20:3186–3190

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Morozova O, Marra M (2008) Applications of next-generation sequencing technologies in functional genomics. Genomics 92:255–264

    Article  PubMed  CAS  Google Scholar 

  • Muthamilarasan M, Prasad M (2015) Advances in Setaria genomics for genetic improvement of cereals and bioenergy grasses. Theor Appl Genet 128:1–14

    Article  PubMed  CAS  Google Scholar 

  • Muthamilarasan M, Theriappan P, Prasad M (2013) Recent advances in crop genomics for ensuring food security. Curr Sci 105:155–158

    Google Scholar 

  • Neumann PM (2008) Coping mechanisms for crop plants in drought-prone environments. Ann Bot 101:901–907

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Osakabe Y, Osakabe K, Shinozaki K, Tran L-SP (2014) Response of plants to water stress. Front Plant Sci 5:86

    Article  PubMed Central  PubMed  Google Scholar 

  • Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible W-R (2009) Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol 150:1541–1555

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Paoletti E, Contran N, Bernasconi P, Günthardt-Goerg MS, Wollenveider P (2010) Structural and physiological responses to ozone in Manna ash (Fraxinus ornus L.) leaves of seedlings and mature trees under controlled and ambient condition. Sci Total Environ 408:2014–2024

    Article  PubMed  CAS  Google Scholar 

  • Qi X, Xie S, Liu Y, Yi F, Yu J (2013) Genome-wide annotation of genes and noncoding RNAs of foxtail millet in response to simulated drought stress by deep sequencing. Plant Mol Biol 83:459–473

    Article  PubMed  CAS  Google Scholar 

  • Qie L, Jia G, Zhang W, Schnable J, Shang Z, Li W, Liu B, Li M, Chai Y, Zhi H, Diao X (2014) Mapping of quantitative trait locus (QTLs) that contribute to germination and early seedling drought tolerance in the interspecific cross Setaria italica x Setaria viridis. PLoS One 9:e101868

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20:3407–3425

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Razmjoo K, Heydarizadeh P, Sabzalian MR (2008) Effect of salinity and drought stresses on growth parameters and essential oil content of Matricaria chamomile. Int J Agric Biol 10:451–454

    Google Scholar 

  • Reyes JL, Chua NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 49:592–606

    Article  PubMed  CAS  Google Scholar 

  • Richmond AT, Somerville CR (2000) The cellulose synthase superfamily. Plant Physiol 124:495–498

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Schreiber AW, Shi B-J, Huang CY, Langridge P, Baumann U (2011) Discovery of barley miRNAs through deep sequencing of short reads. BMC Genom 12:129

    Article  CAS  Google Scholar 

  • Seifert GJ, Blaukopf C (2010) Irritable walls: the plant extracellular matrix and signaling. Plant Physiol 153:467–478

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sheng L, Chai W, Gong X, Zhou L, Cai R, Li X (2015) Identification and characterization of novel maize mirnas involved in different genetic background. Int J Biol Sci 11:781–793

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Skirycz A, Inzé D (2010) More from less: plant growth under limited water. Curr Opin Biotechnol 21:197–203

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sunkar R, Kapoor A, Zhu J (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  PubMed Central  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  PubMed  CAS  Google Scholar 

  • Wang T, Chen L, Zhao M, Tian Q, Zhang W (2011) Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genom 12:367

    Article  CAS  Google Scholar 

  • Wei L, Zhang D, Xiang F, Zhang Z (2009) Differentially expressed miRNAs potentially involved in the regulation of defense mechanism to drought stress in maize seedlings. Int J Plant Sci 170:979–989

    Article  CAS  Google Scholar 

  • Xu L, Wang LJ, Gong YQ, Dai WH, Wang Y, Zhu XW, Wen TC, Liu LW (2012) Genetic linkage map construction and QTL mapping of cadmium accumulation in radish (Raphanus sativus L.). Theor Appl Genet 125:659–670

    Article  PubMed  CAS  Google Scholar 

  • Xu L, Wang Y, Zhai L, Xu Y, Wang L, Zhu X, Gong Y, Yu R, Limera C, Liu L (2013) Genome-wide identification and characterization of cadmium-responsive microRNAs and their target genes in radish (Raphanus sativus L.) roots. J Exp Bot 64:4271–4287

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  PubMed  CAS  Google Scholar 

  • Yang F, Liang G, Liu D, Yu D (2009) Arabidopsis miR396 mediates the development of leaves and flowers in transgenic tobacco. J Plant Biol 52:475–481

    Article  CAS  Google Scholar 

  • Yang J, Liu X, Xu B, Zhao N, Yang X, Zhang M (2013) Identification of miRNAs and their targets using high-throughput sequencing and degradome analysis in cytoplasmic male-sterile and its maintainer fertile lines of Brassica juncea. BMC Genom 14:9

    Article  CAS  Google Scholar 

  • Yi F, Xie S, Liu Y, Qi X, Yu J (2013) Genome-wide characterization of microRNA in foxtail millet (Setaria italica). BMC Plant Biol 13:212

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zabotin AI, Barisheva TS, Zabotina OA, Larskaya IA, Lozovaya VV, Beldman G, Voragen AGJ (1998) Alterations in cell walls of winter wheat roots during low temperature acclimation. J Plant Physiol 152:473–479

    Article  CAS  Google Scholar 

  • Zeng Q-Y, Yang C-Y, Ma Q-B, Li X-P, Dong W-W, Nian H (2012) Identification of wild soybean miRNAs and their target genes responsive to aluminum stress. BMC Plant Biol 12:182

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhang B (2015) MicroRNA: a new target for improving plant tolerance to abiotic stress. J Exp Bot 66:1749–1761

    Article  PubMed  CAS  Google Scholar 

  • Zhang B, Pan X, Cannon C, Cobb G, Anderson T (2006a) Conservation and divergence of plant microRNA genes. Plant J 46:243–259

    Article  PubMed  CAS  Google Scholar 

  • Zhang B, Pan X, Cox S, Cobb G, Anderson T (2006b) Evidence that miRNAs are different from other RNAs. Cell Mol Life Sci 63:246–254

    Article  PubMed  CAS  Google Scholar 

  • Zhang B, Pan X, Anderson TA (2006c) Identification of 188 conserved maize microRNAs and their targets. FEBS Lett 580:3753–3762

    Article  PubMed  CAS  Google Scholar 

  • Zhang JP, Liu TS, Fu JJ, Zhu Y, Jia JP, Zheng J, Zhao YH, Zhang Y, Wang GY (2007) Construction and application of EST library from Setaria italica in response to dehydration stress. Genomics 90:121–131

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Xu Y, Huan Q, Chong K (2009) Deep sequencing of Brachypodium small RNAs at the global genome level identifies microRNAs involved in cold stress response. BMC Genom 10:449

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zhou ZS, Song JB, Yang ZM (2012a) Genome-wide identification of Brassica napus microRNAs and their targets in response to cadmium. J Exp Bot 63:4597–4613

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhou ZS, Zeng HQ, Liu ZP, Yang ZM (2012b) Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant Cell Environ 35:86–99

    Article  PubMed  Google Scholar 

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Acknowledgments

Authors’ work in the area of foxtail millet genomics is supported by the Core Grant of National Institute of Plant Genome Research, New Delhi, India. Ms. Amita Yadav acknowledges the Research Fellowship received from Council of Scientific and Industrial Research (CSIR), New Delhi, India.

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Correspondence to Manoj Prasad.

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Yadav, A., Khan, Y. & Prasad, M. Dehydration-responsive miRNAs in foxtail millet: genome-wide identification, characterization and expression profiling. Planta 243, 749–766 (2016). https://doi.org/10.1007/s00425-015-2437-7

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