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Genome-wide identification and characterization of drought responsive MicroRNAs in Solanum tuberosum L.

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Abstract

MicroRNAs (miRNAs) are small non-coding RNAs that function as negative post-transcriptional regulators during plant growth and development in response to biotic and abiotic stresses. The objective of this study was to use next-generation sequencing (miRNA-sequencing) technology to identify drought responsive miRNAs from potato (Solanum tuberosum L.). After inducing small RNA under experimental conditions of aeration without watering for 1, 3, and 6 h compared to those at 0 h control, NGS was used to identify drought responsive miRNAs. From these drought responsive miRNAs, 21 known miRNAs and 19 novel miRNAs were selected. Of them, 38 were subjected to expression level analysis under four abiotic stresses (drought, salt, cold and abscisic acid) treatment through northern blot while two novel miRNAs were subjected to quantitative reverse transcription PCR (qRT-PCR) to determine their expression levels. The effects of other abiotic stresses such as cold, salt, and ABA treatments on the expression levels of the 38 drought responsive miRNAs were also analyzed. Putative target gene regulatory network of novel miRNAs were determined through computational analysis.

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References

  • Allen E, Xie Z, Gustafson AM, Sung GH, Spatafora JW, Carrington JC (2004) Evolution of microRNA genes by inserted duplication of target gene sequences in Arabidopsis thaliana. RAN. Nat Genet 36:1282–1290

    Article  CAS  PubMed  Google Scholar 

  • Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC, Licausi F, Perata P, Voesenek LA, Dongen JT (2012) Making sense of low oxygen sensing. Trends Plant Sci 17:129–138

    Article  CAS  PubMed  Google Scholar 

  • Banks IR, Zhang Y, Wiggins BE, Heck GR, Ivashuta S (2012) RNA decoys: an emerging component of plant regulatory networks? Plant Signal Behav 7:1188–1193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Lin HJ, Pan GT, Zhang ZM, Zhang B, Shen YO, Qin C, Zhang Q, Zhao MJ (2010) Identification of known microRNAs in root and leaf of maize by deep sequencing. Artic Chinese Yi Chuan 32:1175–1186

    Google Scholar 

  • Covarrubias AA, Reyes JL (2010) Post-transcriptional gene regulation of salinity and drought responses by plant microRNAs. Plant Cell Environ 33:481–489

    Article  CAS  PubMed  Google Scholar 

  • Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163–177

    Article  PubMed  PubMed Central  Google Scholar 

  • Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39(suppl 2):W155–W159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ebrahimi Khaksefidi R, Mirlohi S, Khalaji F, Fakhari Z, Shiran B, Fallahi H, Rafiei F, Budak H, Ebrahimie E (2015) Differential expression of seven conserved microRNAs in response to abiotic stress and their regulatory network in Helianthus annuus. Front Plant Sci 6:741

    Article  PubMed  PubMed Central  Google Scholar 

  • Friedländer MR, Mackowiak SD, Li N, Chen W, Rajewsky N (2012) miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res 40:37–52

    Article  PubMed  Google Scholar 

  • Guerra D, Crosatti C, Khoshro HH, Mastrangelo AM, Mica E, Mazzucotelli E (2015) Post-transcriptional and post-translational regulations of drought and heat response in plants: a spider’s web of mechanisms. Front Plant Sci 6:57

    Article  PubMed  PubMed Central  Google Scholar 

  • Howell SH (2013) Endoplasmic reticulum stress responses in plants. Annu Rev Plant Biol 64:477–499

    Article  CAS  PubMed  Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403

    Article  CAS  PubMed  Google Scholar 

  • Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Do Choi Y, Kim M, Reuzeau C, Kim JK (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kim J, Jung JH, Reyes JL, Kim YS, Kim SY, Chung KS, Kim JA, Lee M, Lee Y, Narry Kim V (2005) MicroRNA-directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. Plant J 42:84–94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim JJ, Lee JH, Kim W, Jung HS, Huijser P, Ahn JH (2012) The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 Module Regulates Ambient Temperature-Responsive Flowering via FLOWERING LOCUS T in Arabidopsis. Plant Physiol 159:461–478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohli D, Joshi G, Deokar AA, Bhardwaj AR, Agarwal M, Katiyar-Agarwal S, Srinivasan R, Jain PK (2014) Identification and characterization of Wilt and salt stress-responsive microRNAs in chichkpea through high-throughput sequencing. PLoS ONE 9:e108851

    Article  PubMed  PubMed Central  Google Scholar 

  • Kozomara A, Griffiths-Jones S (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42:D68–D73

    Article  CAS  PubMed  Google Scholar 

  • Krishnaswamy SS, Srivastava S, Mohammadi M, Rahman MH, Deyholos MK, Kav NAV (2008) Transcriptional profiling of pea ABR17 mediated changes in gene expression in Arabidopsis thaliana. BMC Plant Biol 8:91

    Article  PubMed  PubMed Central  Google Scholar 

  • Langmead B, TrapnellnC, Pop M, Salzberq SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee BH, Henderson DA, Zhu JK (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Rice JH, Chen N, Baum TJ, Hewezi T (2014) Synchronization of developmental processes and defense signaling by growth regulating transcription factors. PLoS ONE 9:e98477

    Article  PubMed  PubMed Central  Google Scholar 

  • Lyzenga WF, Stone SL (2012) Abiotic stress tolerance mediated by protein ubiquitination. J Exp Bot 63:599–616

    Article  CAS  PubMed  Google Scholar 

  • Murchison EP, Hannon GJ (2004) miRNAs on the move: miRNA biogenesis and the RNAi machinery. Curr Opin Cell Biol 16:223–229

    Article  CAS  PubMed  Google Scholar 

  • Phlilips JR, Dalmay T, Bartels D (2007) The role of small RNAs in abiotic stress. FEBS Lett 581:3592–3597

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reichel M, Millar AA (2015) Specificity of plant microRNA target MIMICs: cross-targeting of miR159 and miR319. J Plant Physiol 180:45–48

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520

    Article  CAS  PubMed  Google Scholar 

  • Ronen R, Gan I, Modai S, Sukacheov A, Dror G, Halperin E, Shomron N (2010) miRNAkey: a software for microRNA deep sequencing analysis. Bioinformatics 26:2615–2616

    Article  CAS  PubMed  Google Scholar 

  • Saito R, Smoot ME, Ono K, Ruscheinski J, Wang PL, Lotia S, Pico AR, Bader GD, Ideker T (2012) A travel guide to Cytoscape plug-ins. Nat Methods 9:1069–1076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silveira RD, Abreu FR, Mamidi S, McClean PE, Vianello RP, Lanna AC, Carneiro NP, Brondani C (2015) Expression of drought tolerance genes in tropical upland rice cultivars (Oryza sativa). Genet Mol Res 14:8181–8200

    Article  CAS  PubMed  Google Scholar 

  • Sun Z, Evans J, Bhagwate A, Middha S, Bockol M, Yan H, Kocher JP (2014) CAP-miRSeq: a comprehensive analysis pipeline for microRNA sequencing data. BMC Genom 15:423

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunkar R, Li YF, Jagadeeswaran G (2012) Function of microRNAs in plant stress responses. Trends Plant Sci 17:196–203

    Article  CAS  PubMed  Google Scholar 

  • Turner M, Yu O, Subramanian S (2012) Genome organization and characteristics of soybean microRNAs. BMC Genom 13:169

    Article  CAS  Google Scholar 

  • Wang D, Pan Y, Zhao X, Zhu L, Fu B, Li Z (2011) Genome-wide temporal-spatial gene expression profiling of drought responsiveness in rice. BMC Genom 12:149–164

    Article  Google Scholar 

  • Wollmann H, Mica E, Todesco M, Long JA, Weigel D (2010) On reconciling the interactions between APETALA2, miR172 and AGAMOUS with the ABC model of flower development. Development 137:3633–3642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu C, Yang RF, Li WC, Fu FL (2010) Identification of 21 microRNAs in maize and their differential expression under drought stress. Afr J Biotechnol 9:4741–4753

    Google Scholar 

  • Yamaguchi A, Wu MF, Yang L, Wu G, Poethig RS, Wagner D (2009) The MicroRNA-regulated SBP-Box transcription factor SPL3 Is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 17:268–278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi M, Goue N, Igarashi H, Ohtani M, Nakano Y, Mortimer JC, Nishikubo N, Kubo M, Katayama Y, Kakegawa K, Dupree P, Demura T (2010) VASCULAR-RELATED NAC-DOMAIN6 (VND6) and VND7 effectively induce transdifferentiation into xylem vessel elements under control of an induction system. Plant Physiol 153:915–924

    Article  Google Scholar 

  • Yang X, Tu L, Zhu L, Fu L, Min L, Zhang X (2008) Expression profile analysis of genes involved in cell wall regeneration during protoplast culture in cotton by suppression subtractive hybridization and microarray. J Exp Bot 59:3661–3674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang FX, Zhu GF, Wang Z, Liu HL, Huang D (2015) A putative miR172-targeted CeAPETALA2-like gene is involved in floral patterning regulation of the orchid Cymbidium ensifolium. Genet Mol Res 14:12049–12061

    Article  CAS  PubMed  Google Scholar 

  • Zeng C, Wang W, Zheng Y, Chen X, Bo W, Song S, Zhang W, Peng M (2010) Conservation and divergence of microRNAs and their functions in Euphorbiaceous plants. Nucleic Acids Res 38:981–995

    Article  CAS  PubMed  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by a Sunmoon University Research Grant of 2016.

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This work was supported by a Sunmoon University Research Grant of 2016.

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Correspondence to Hawk-Bin Kwon.

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Seon-Ju Shin declares that she does not have conflict of interest. Jae-Hee Lee declares that she does not have conflict of interest. Hawk-Bin Kwon declares that he does not have conflict of interest.

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Shin, SJ., Lee, JH. & Kwon, HB. Genome-wide identification and characterization of drought responsive MicroRNAs in Solanum tuberosum L.. Genes Genom 39, 1193–1203 (2017). https://doi.org/10.1007/s13258-017-0586-8

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