Emerging techniques to decipher microRNAs (miRNAs) and their regulatory role in conferring abiotic stress tolerance of plants
Tóm tắt
MicroRNAs (miRNAs) are a distinct class of non-coding, small regulatory RNAs which have evolved significantly in generating abiotic stress tolerance across a variety of model plants and crop species. These miRNAs, while undergoing post-transcriptional modifications, have often been found to be linked with epigenetic regulations of stress-responsive gene expression. The discovery of isomers of miRNAs (isomiRs) is also a remarkable event, as some schools of scientists believe them to be regulatory molecules distinct from the conventional miRNAs. The link between isomiRs and abiotic stress responses in plants is now a field of intense research. In this review, we have highlighted the mechanism of various tools and techniques which are essential to visualize high-throughput data analysis. Such data are required for generating large-scale libraries of small RNAs, from which stress-responsive miRNAs are conventionally screened. The concluding part of the review especially contains an exhaustive discussion on the recent developments of miRNA-mediated tolerance towards multiple stresses, such as nutrient deficiency, salinity, drought, oxidative stress, hypoxia, temperature stress, radiation, and heavy metal toxicity. Both transgenic as well as miRNAome approaches have been focussed in this section of the review.
Tài liệu tham khảo
Abdel-Ghany SE, Pilon M (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283:15932–15945
Ali N, Datta SK, Datta K (2010) RNA interference in designing transgenic crops. GM Crops 1:207–213
Alonso C, Pérez R, Bazaga P, Medrano M, Herrera CM (2015) MSAP markers and global cytosine methylation in plants: a literature survey and comparative analysis for a wild growing species. Mol Ecol Resour. doi:10.1111/1755-0998.12426
An J, Lai J, Lehman ML, Nelson CC (2013) miRDeep*: an integrated application tool for miRNA identification from RNA sequencing data. Nucleic Acids Res 41:727–737
Anders S, Pyl PT, Huber W (2014) HTSeq—a Python framework to work with high throughput sequencing data. Bioinformatics 2014:1–4
Arenas-Huertero C, Pérez B, Rabanal F, Blanco-Melo D, De la Rosa C, Estrada-Navarrete G et al (2009) Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol Biol 70:385–401
Ares M (2011) Methods for processing high-throughput RNA sequencing data. Adapted from RNA: a laboratory manual by Donald C. Rio, Manuel Ares Jr, Gregory J. Hannon, and Timothy W. Nilsen. CSHL Press, Cold Spring Harbor, NY, USA
Baek D, Kim MC, Chun HJ, Kang S, Park HC, Shin G et al (2013) Regulation of miR399f transcription by AtMYB2 affects phosphate starvation responses in Arabidopsis. Plant Physiol 161:362–373
Banerjee A, Roychoudhury A (2015) Abscisic-acid-dependent basic leucine zipper (bZIP) transcription factors in plant abiotic stress. Protoplasma. doi:10.1007/s00709-015-0920-4
Banerjee A, Roychoudhury A (2016) Group II late embryogenesis abundant (LEA) proteins: structural and functional aspects in plant abiotic stress. Plant Growth Regul 79:1–17
Barciszewska-Pacak M, Milanowska K, Knop K, Bielewicz D, Nuc P, Plewka P et al (2015) Arabidopsis microRNA expression regulation in a wide range of abiotic stress responses. Front Plant Sci 6:410
Basak J, Nithin C (2015) Targeting non-coding RNAs in plants with the CRISPR-Cas technology is a challenge yet worth accepting. Front Plant Sci 6:1001
Bhardwaj AR, Joshi G, Pandey R, Kukreja B, Goel S, Jagannath A et al (2014) A genome-wide perspective of miRNAome in response to high temperature, salinity and drought stresses in Brassica juncea (Czern) L. PLoS One 9:e92456
Bielewicz D, Kalak M, Kalyna M, Windels D, Barta A, Vazquez F, Szweykowska-Kulinska Z, Jarmolowski A (2013) Introns of plant pri-miRNAs enhance miRNA biogenesis. EMBO Rep 14:622–628
Bonnet E, He Y, Billiau K, Vande Peer Y (2010) TAPIR, a webserver for the prediction of plant microRNA targets, including target mimics. Bioinformatics 26:1566–1568
Bukhari SA, Shang S, Zhang M, Zheng W, Zhang G, Wang TZ et al (2015) Genome-wide identification of chromium stress-responsive micro RNAs and their target genes in tobacco (Nicotiana tabacum) roots. Environ Toxicol Chem 34:2573–2582
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 Genomics 16:692
Chen L, Luan Y, Zhai J (2015) Sp-miR396a-5p acts as a stress-responsive genes regulator by conferring tolerance to abiotic stresses and susceptibility to Phytophthora nicotianae infection in transgenic tobacco. Plant Cell Rep 34:2013–2025
Chou C-H, Chang N-W, Shrestha S, Hsu S-D, Lin Y-L, Lee W-H et al (2015) miRTarBase 2016: updates to the experimentally validated miRNA-target interactions database. Nucleic Acids Res 2015:1–9
Ci D, Song Y, Tian M, Zhang D (2015) Methylation of miRNA genes in the response to temperature stress in Populus simonii. Front Plant Sci 6:921
Cui H, Zhai J, Ma C (2015a) miRLocator: machine learning-based prediction of mature microRNAs within plant pre-miRNA sequences. PLoS One 10:e0142753
Cui LG, Shan JX, Shi M, Gao JP, Lin HX (2015b) The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants. Plant J 80:1108–1117
Davy A, Thomsen KK, Juliano MA, Alves LC, Svendsen I, Simpson DJ (2000) Purification and characterization of barley dipeptidyl peptidase IV. Plant Physiol 122:425–432
de Oliveira LF, Christoff AP, Margis R (2013) isomiRID: a frame work to identify microRNA isoforms. Bioinformatics 29:2521–2523
Denman R (1993) Using RNAFOLD to predict the activity of small catalytic RNAs. Biotechniques 15:1090–1095
Ding SW, Voinnet O (2007) Antiviral immunity directed by small RNAs. Cell 30:413–426
Friedländer MR, Chen W, Adamidi C, Maaskola J, Einspanier R, Knespel S et al (2008) Discovering microRNAs from deep sequencing data using miRDeep. Nat Biotechnol 26:407–415
Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S et al (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80
German MA, Luo S, Schroth G, Meyers BC, Green PJ (2009) Construction of Parallel Analysis of RNA Ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome. Nat Protoc 4:356–362
Gharat SA, Shaw BP (2015) Novel and conserved miRNAs in the halophyte Suaeda maritima identified by deep sequencing and computational predictions using the ESTs of two mangrove plants. BMC Plant Biol 15:301
Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proc Natl Acad Sci U S A 105:803–808
Golldack D, Luking I, Yang O (2011) Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Rep 30:1383–1391
Gordon A, Hannon G (2010) Fastx-toolkit. FASTQ/A Short-reads Pre-processing Tools. Unpublished available online at: http://hannonlab.cshl.edu/fastx_toolkit
Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G et al (2010) Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. Physiol Plant 138:226–237
Hackenberg M, Shi BJ, Gustafson P, Langridge P (2013) Characterization of phosphorus-regulated miR399 and miR827 and their isomirs in barley under phosphorus-sufficient and phosphorus-deficient conditions. BMC Plant Biol 13:214
Hajyzadeh M, Turktas M, Khawar KM, Unver T (2015) miR408 overexpression causes increased drought tolerance in chickpea. Gene 555:186–193
He Q, Zhu S, Zhang B (2014) MicroRNA–target gene responses to lead induced stress in cotton (Gossypium hirsutum L.). Funct Integr Genomics 14:507–515
Huang SQ, Xiang AL, Che LL, Chen S, Li H, Song JB, Yang ZM (2010) A set of miRNAs from Brassica napus in response to sulphate deficiency and cadmium stress. Plant Biotechnol J 8:887–899
Huang CY, Shirley N, Genc Y, Shi B, Langridge P (2011) Phosphate utilization efficiency correlates with expression of low-affinity phosphate transporters and noncoding RNA, IPS1, in barley. Plant Physiol 156:1217–1229
Jia X, Ren L, Chen Q-J, Li R, Tang G (2009) UV-B-responsive microRNAs in Populus tremula. J Plant Physiol 166:2046–2057
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799
Joo HJ, Kim KY, Yim YH, Jin YX, Kim H, Kim MY et al (2010) Contribution of the peroxisomal acox gene to the dynamic balance of daumone production in Caenorhabditis elegans. J Biol Chem 285:29319–29325
Jung HJ, Kang H (2007) Expression and functional analyses of microRNA417 in Arabidopsis thaliana under stress conditions. Plant Physiol Biochem 45:805–811
Kadri S, Hinman V, Benos PV (2009) HHMMiR: efficient de novo prediction of microRNAs using hierarchical hidden Markov models. BMC Bioinform 10:S35
Kansal S, Devi RM, Balyan SC, Arora MK, Singh AK et al (2015) Unique miRNome during anthesis in drought-tolerant indica rice var. Nagina 22. Planta 241:1543–1559
Kant S, Peng M, Rothstein SJ (2011) Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasisin Arabidopsis. PLoS Genet 7:e1002021
Kawashima CG, Matthewman CA, Huang S, Lee BR, Yoshimoto N, Koprivova A et al (2011) Interplay of SLIM1 and miR395 in the regulation of sulphate assimilation in Arabidopsis. Plant J 66:863–876
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
Khraiwesh B, Arif MA, Seumel GI, Ossowski S, Weigel D, Reski R, Frank W (2010) Transcriptional control of gene expression by microRNAs. Cell 140:111–122
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
Kruszka K, Pacak A, Swida-Barteczka Nuc P, Alaba S, Wroblewska Z et al (2014) Transcriptionally and post-transcriptionally regulated microRNAs in heat stress response in barley. J Exp Bot 65:6123–6135
Lager I, Yilmaz JL, Zhou XR, Jasieniecka K, Kazachkov M, Wang P et al (2013) Plantacyl-CoA: lysophosphatidylcholine acyltransferases (LPCATs) have different specificities in their forward and reverse reactions. J Biol Chem 288:36902–36914
Lawrence M, Huber W, Pagès H, Aboyoun P, Carlson M, Gentleman R, Morgan MT, Carey VJ (2013) Software for computing and annotating genomic ranges. PLoS Comput Biol 9:e1003118
Leaman R, Gonzalez G (2008) BANNER: an executable survey of advances in biomedical named entity recognition. Pac Symp Biocomput 2008:652–663
Leclercq M, Diallo AB, Blanchette M (2013) Computational prediction of the localization of microRNAs within their pre-miRNA. Nucleic Acids Res 2013:1–12
Lee WS, Gudimella R, Wong GR, Tammi MT, Khalid N, Harikrishna JA (2015) Transcripts and microRNAs responding to salt stress in Musa acuminata Colla (AAA Group) cv. Berangan roots. PLoS One 10:e0127526
Li T, Li H, Zhang Y-X, Liu J-Y (2011) Identification and analysis of seven H2O2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica). Nucleic Acids Res 39:2821–2833
Li B, Duan H, Li J, Deng XW, Yin W, Xia X (2013) Global identification of miRNAs and targets in Populus euphratica under salt stress. Plant Mol Biol 81:525–539
Li G, Ross KE, Arighi CN, Peng Y, Wu CH, Vijay-Shanker K (2015) miRTex: a text mining system for miRNA-gene relation extraction. PLoS Comput Biol 11:e1004391
Li W, Wang T, Zhang Y, Li Y (2016) Overexpression of soybean miR172c confers tolerance to water deficit and salt stress, but increases ABA sensitivity in transgenic Arabidopsis thaliana. J Exp Bot 67:175–194
Liang G, He H, Yu D (2012) Identification of nitrogen starvation-responsive miRNAs in Arabidopsis thaliana. PLoS One 7:e48951
Liao Y, Smyth GK, Shi W (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930
Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52:133–146
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 Lett 583:723–728
Liu H, Searle IR, Mather DE, Able AJ, Able JA (2015a) Morphological, physiological and yield responses of durum wheat to pre-anthesis water deficit stress are genotype-dependent. Crop Pasture Sci 66:1024–1038
Liu H, Searle IR, Watson-Haigh NS, Baumann U, Mather DE, Able AJ et al (2015b) Genome-wide identification of microRNAs in leaves and the developing head of four durum genotypes during water deficit stress. PLoS One 10:e0142799
Love MI, Anders S, Kim V, Huber W (2015) RNA-Seq workflow: gene-level exploratory analysis and differential expression. F1000 Res 4:1070
Lu C, Fedoroff N (2000) A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell 12:2351–2366
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
Lundmark M, Korner CJ, Nielsen TH (2010) Global analysis of microRNA in Arabidopsis in response to phosphate starvation as studied by locked nucleic acid-based microarrays. Physiol Plant 140:57–68
Ma C, Burd S, Lers A (2015) miR408 is involved in abiotic stress responses in Arabidopsis. Plant J 84:169–187
Matthewman CA, Kawashima CG, Huska D, Csorba T, Dalmay T, Kopriva S (2012) miR395 is a general component of the sulphate assimilation regulatory network in Arabidopsis. FEBS Lett 586:3242–3248
Mohorianu I, Stocks MB, Wood J, Dalmay T, Moulton V (2013) CoLIde: a bioinformatics tool for CO-expression based smallRNA loci identification using high-throughput sequencing data. RNA Biol 10:1221–1230
Moldovan D, Spriggs A, Yang J, Pogson BJ, Dennis ES, Wilson IW (2009) Hypoxia responsive microRNAs and trans-acting small interfering RNAs in Arabidopsis. J Exp Bot 61:165–177
Morin RD, Aksay G, Dolgosheina E, Ebhardt HA, Magrini V, Mardis ER et al (2008) Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Res 18:571–584
Moxon S, Schwach F, Dalmay T, Maclean D, Studholme DJ, Moulton V (2008) A toolkit for analysing large-scale plant small RNA datasets. Bioinformatics 24:2252–2253
Mullen MA, Assmann SM, Bevilacqua PC (2012) Toward a digital gene response: RNA G-quadruplexes with fewer quartets fold with higher cooperativity. J Am Chem Soc 134:812–815
Muller H, Marzi MJ, Nicassio F (2014) IsomiRage: from functional classification to differential expression of miRNA isoforms. Front Bioeng Biotechnol 2:38
Nigam D, Kumar S, Mishra DC, Rai A, Smita S, Saha A (2015) Synergistic regulatory networks mediated by microRNAs and transcription factors under drought, heat and salt stresses in Oryza sativa spp. Gene 555:127–139
Nordström K, Wagner EG (1994) Kinetic aspects of control of plasmid replication by antisense RNA. Trends Biochem Sci 19:294–300
Numnark S, Mhuantong W, Ingsriswang S, Wichadakul D (2012) C-mii: a tool for plant miRNA and target identification. BMC Genomics 13:S16
Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–738
Pant BD, Musialak-lange M, Nuc P, May P, Buhtz A, Kehr J et al (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
Patel RK, Jain M (2012) NGSQC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS One 7:e30619
Patra D, Fasold M, Lagenberger D, Steger G, Grosse I, Stadler PF (2014) plantDARIO: web based quantitative and qualitative analysis of small RNA-seq data in plants. Front Plant Sci 5:708
Paul S, Datta SK, Datta K (2015) miRNA regulation of nutrient homeostasis in plants. Front Plant Sci 6:232
Peng Y, Torii M, Wu CH, Vijay-Shanker K (2014) A generalizable NLP framework for fast development of pattern-based biomedical relation extraction systems. BMC Bioinform 15:285
Raghuram B, Sheikh H, Sinha AK (2014) Regulation of MAP kinase signaling cascade by microRNAs in Oryza sativa. Plant Signal Behav 9:e972130
Rakei A, Maali-Amiri R, Zeinali H, Ranjbar M (2016) DNA methylation and physio-biochemical analysis of chickpea in response to cold stress. Protoplasma 253:61–76
Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10:503–509
Reddy AS, Marquez Y, Kalyna M, Barta A (2013) Complexity of the alternative splicing landscape in plants. Plant Cell 25:3657–3683
Reyes JL, Chua N-H (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 49:592–606
Roychoudhury A, Banerjee A (2015) Transcriptome analysis of abiotic stress response in plants. Transcriptomics 3:2
Roychoudhury A, Paul S, Basu S (2013) Cross-talk between abscisic acid-dependent and abscisic acid-independent pathways during abiotic stress. Plant Cell Rep 32:985–1006
Roychoudhury A, Banerjee A, Lahiri V (2015) Metabolic and molecular-genetic regulation of proline signaling and its cross-talk with major effectors mediates abiotic stress tolerance in plants. Turk J Bot 39:887–910
Rueda A, Barturen G, Lebrón R, Gómez-Martín C, Alganza Á, Oliver JL et al (2015) sRNA toolbox: an integrated collection of small RNA research tools. Nucleic Acids Res 43:W467–W473
Rzezniczak TZ, Merritt TJ (2012) Interactions of NADP-reducing enzymes across varying environmental conditions: a model of biological complexity. G3 (Bethesda) 2:1613–1623
Sablok G, Milev I, Minkov G, Minkov I, Varotto C, Yahubyan G et al (2013) isomiRex: web-based identification of microRNAs, isomiR variations and differential expression using next-generation sequencing datasets. FEBS Lett 587:2629–2634
Sablok G, Srivastva AK, Suprasanna P, Baev V, Ralph PJ (2015) isomiRs: increasing evidences of isomiRs complexity in plant stress functional biology. Front Plant Sci 6:949
Sharma N, Tripathi A, Sanan-Mishra N (2015) Profiling the expression domains of a rice-specific microRNA under stress. Front Plant Sci 6:333
Shin S-Y, Shin C (2016) Regulatory non-coding RNAs in plants: potential gene resources for the improvement of agricultural traits. Plant Biotechnol Rep 10:35–47
Sobkowiak L, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z (2012) Non-canonical processing of Arabidopsis pri-miR319a/b/c generates additional microRNAs to target one RAP2.12 mRNA isoform. Front Plant Sci 3:46
Song YP, Ci D, Tian M, Zhang DQ (2014) Comparison of the physiological effects and transcriptome responses of Populus simonii under different abiotic stresses. Plant Mol Biol 86:139–156
Sun X, Fan G, Su L, Wang W, Liang Z, Li S, Xin H (2015a) Identification of cold-inducible microRNAs in grapevine. Front Plant Sci 6:595
Sun X, Xu L, Wang Y, Yu R, Zhu X, Luo X, Gong Y (2015b) Identification of novel and salt-responsive miRNAs to explore miRNA-mediated regulatory network of salt stress response in radish (Raphanus sativus L.). BMC Genomics 16:197
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019
Sunkar R, Girke T, Jain PK, Zhu JK (2005) Cloning and characterization of microRNAs from rice. Plant Cell 17:1397–1411
Sunkar R, Kapoor A, Zhu JK (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
Szarzynska B, Sobkowiak L, Pant BD, Balazadeh S, Scheible WR, Mueller-Roeber B, Jarmolowski A, Szweykowska-Kulinska Z (2009) Gene structures and processing of Arabidopsis thaliana HYL1-dependent pri-miRNAs. Nucleic Acids Res 37:3083–3093
Teune J-H, Steger G (2010) NOVOMIR: de novo prediction of microRNA-coding regions in a single plant-genome. J Nucleic Acids 2010:495904
Tian H, Jia Y, Niu T, Yu Q, Ding Z (2014) The key players of the primary root growth and development also function in lateral roots in Arabidopsis. Plant Cell Rep 33:745–753
Tian C, Zuo Z, Qiu JL (2015) Identification and characterization of ABA-responsive microRNAs in rice. J Genet Genomics 42:393–402
Tripathi A, Goswami K, Sanan-Mishra N (2015) Role of bioinformatics in establishing microRNAs as modulators of abiotic stress responses: the new revolution. Front Physiol 6:286
Unver T, Namuth-Covert DM, Budak H (2009) Review of current methodological approaches for characterizing microRNAs in plants. Int J Plant Genomics 2009:262463
Vazquez F, Hohn T (2013) Biogenesis and biological activity of secondary siRNAs in plants. Scientifica 2013:783253
Wang Q, Zhang B (2015) MicroRNAs in cotton: an open world needs more exploration. Planta 241:1303–1312
Wang X-C, Zhao Q-Y, Ma C-L, Zhang Z-H, Cao H-L, Kong Y-M et al (2013) Global transcriptome profiles of Camellia sinensis during cold acclimation. BMC Genomics 14:415
Wang Y, Zhao Z, Deng M, Liu R, Niu S, Fan G (2015) Identification and functional analysis of microRNAs and their targets in Platanus acerifolia under lead (Pb) stress. Int J Mol Sci 16:7098–7111
Wolt JD, Wang K, Yang B (2016) The regulatory status of genome-edited crops. Plant Biotechnol J 14:510–518
Wu P, Han S, Zhao W, Chen T, Zhou J, Li L (2015) Genome-wide identification of abiotic stress-regulated and novel microRNAs in mulberry leaf. Plant Physiol Biochem 95:75–82
Wyman SK, Knouf EC, Parkin RK, Fritz BR, Lin DW, Dennis LM et al (2011) Post-transcriptional generation of miRNA variants by multiple nucleotidyl transferases contributes to miRNA transcriptome complexity. Genome Res 21:1450–1461
Xie F, Wang Q, Zhang B (2015) Global microRNA modification in cotton (Gossypium hirsutum L.). Plant Biotechnol J 13:492–500
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
Xu F, Liu Q, Chen L, Kuang J, Walk T, Wang J et al (2013) Genome-wide identification of soybean microRNAs and their targets reveals their organ-specificity and responses to phosphate starvation. BMC Genomics 14:66
Yadav A, Khan Y, Prasad M (2016) Dehydration-responsive miRNAs in foxtail millet: genome-wide identification, characterization and expression profiling. Planta 243:749–766
Yaish MW, Sunkar R, Zheng Y, Ji B, Al-Yahyai R, Farooq SA (2015) A genome wide identification of the miRNAome in response to salinity stress in date palm (Phoenix dactylifera L.). Front Plant Sci 6:946
Yan Z, Hossain MS, Wang J, Valdes-Lopez O, Liang Y, Libault M et al (2013) miR172 regulates soybean nodulation. Mol Plant Microbe Interact 26:1371–1377
Yang X, Li L (2011) miRDeep-P: a computational tool for analyzing the microRNA transcriptome in plants. Bioinformatics 27:2614–2615
Yang ZB, Eticha D, Albacete A, Rao IM, Roitsch T, Horst WJ (2012) Physiological and molecular analysis of the interaction between aluminium toxicity and drought stress in common bean (Phaseolus vulgaris). J Exp Bot 63:3109–3125
Yang R, Zeng Y, Yi X, Zhao L, Zhang Y (2015) Small RNA deep sequencing reveals the important role of microRNAs in the halophyte Halostachys caspica. Plant Biotechnol J 13:395–408
Zhai J, Dong Y, Sun Y, Wang Q, Wang N et al (2014) Discovery and analysis of microRNAs in Leymus chinensis under saline–alkali and drought stress using high-throughput sequencing. PLoS One 9:e105417
Zhang B (2015) MicroRNA: a new target for improving plant tolerance to abiotic stress. J Exp Bot 66:1749–1761
Zhang Z, Wei L, Zou X, Tao Y, Liu Z, Zheng Y (2008) Submergence-responsive microRNAs are potentially involved in the regulation of morphological and metabolic adaptations in maize root cells. Ann Bot 102:509–519
Zhang J, Zhang S, Li S, Han S, Wu T, Li X et al (2013a) A genome-wide survey of micro RNA truncation and 3′ nucleotide addition events in larch (Larix leptolepis). Planta 237:1047–1056
Zhang Q, Zhao C, Li M, Sun W, Liu Y, Xia H et al (2013b) Genome-wide identification of Thellungiella salsuginea microRNAs with putative roles in the salt stress response. BMC Plant Biol 13:180
Zhang S, Yue Y, Sheng L, Wu Y, Fan G, Li A et al (2013c) PASmiR: a literature-curated database for miRNA molecular regulation in plant response to abiotic stress. BMC Plant Biol 13:33
Zhao M, Ding H, Zhu JK, Zhang F, Li W-X (2011) Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytol 190:906–915
Zheng C, Zhao L, Wang Y, Shen J, Zhang Y, Jia S et al (2015) Integrated RNA-Seq and sRNA-Seq analysis identifies chilling and freezing responsive key molecular players and pathways in tea plant (Camellia sinensis). PLoS One 10:e0125031
Zhou M, Luo H (2014) Role of microRNA319 in creeping bentgrass salinity and drought stress response. Plant Signal Behav 9:e28700
Zhou X, Wang G, Zhang W (2007) UV-B responsive microRNA genes in Arabidopsis thaliana. Mol Syst Biol 3:103
Zhou ZS, Huang SQ, Yang ZM (2008) Bioinformatic identification and expression analysis of new microRNAs from Medicago truncatula. Biochem Biophys Res Commun 374:538–542
Zhuang Y, Zhou X-H, Liu J (2014) Conserved miRNAs and their response to salt stress in wild Egg plant Solanum linnaeanum roots. Int J Mol Sci 15:839–849
Zuker M (2003) Mfold webserver for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415