Abstract
MicroRNAs (miRNAs) are endogenous, tiny RNA molecules that sit at the heart of regulating gene expression in numerous developmental and signaling pathways. Recent investigations have revealed that abiotic stresses encourage non-typical expression patterns of several miRNAs, accordingly proposing miRNAs as potent and novel targets for enhancement plant tolerance against abiotic factors. The stress driven miRNA-response is dependent on types of miRNA, stress, tissues or organs as well as plant genotype. The stress responsive miRNAs act either as negative-regulatory entities by down regulating negative regulators for stress tolerance or as positive-regulatory entities approving amassing of positive regulators. The current scenario on miRNA-based research vastly focus on the identification and target prediction/validation of stress-responsive miRNAs along with their functional expression under stress conditions. It has predominately been accomplished with the advent of high throughput sequencing technologies coupled with online databases and tools. However, there is an urge of epigenomics, functional characterization, and expression-pattern studies to illuminate the communal regulatory pathways by miRNAs that trigger abiotic stress tolerance in major crops. The short tandem target mimic (STTM) and genome editing technologies can be exploited for efficient utilization of miRNAs for traits improvement. Beside the classical pathways, non canonical pathways and novel loci of miRNAs origin and their possible role in abiotic stress response need to be deciphered for their effective utilization. Through this review, we are presenting herein a current understanding about plant miRNAs, their biogenesis and involvement in stress-responses and modulation, various tools and databases used for prediction/identification of plant miRNAs and their targets. A perspective analysis on use of miRNAs as potent targets to engineer abiotic stress tolerance in plants has been presented with emphasis on recent developments, challenges and future perspectives.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdelfattah AM, Park C, Choi MY (2014) Update on non-canonical microRNAs. Biomol Concepts 5:275–287. https://doi.org/10.1515/bmc-2014-0012
Aglawe SB, Barbadikar KM, Mangrauthia SK, Madhav MS (2018) New breeding technique “genome editing” for crop improvement: applications, potentials and challenges. 3 Biotech 8:336. https://doi.org/10.1007/s13205-018-1355-3
Akdogan G, Tufekci ED, Uranbey S, Unver T (2015) miRNA-based drought regulation in wheat. Funct Integr Genomics 16:221–233. https://doi.org/10.1007/s10142-015-0452-1
Al Abdallat AM, Ayad JY, Abu Elenein JM, Al Ajlouni Z, Harwood WA (2014) Overexpression of the transcription factor HvSNAC1 improves drought tolerance in barley (Hordeum vulgare L.). Mol Breed 33:401–414. https://doi.org/10.1007/s11032-013-9958-1
Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221. https://doi.org/10.1016/j.cell.2005.04.004
Amor BB, Wirth S, Merchan F, Laporte P, Aubenton-Carafa Y, Hirsch J, Maizel A, Mallory A, Lucas A, Deragon JM, Vaucheret H, Thermes C, Crespi M (2009) Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res 19:57–69. https://doi.org/10.1101/gr.080275.108
An J, Lai J, Sajjanhar A, Lehman ML, Nelson CC (2014) miRPlant: an integrated tool for identification of plant miRNA from RNA sequencing data. BMC Bioinformatics 15:275. https://doi.org/10.1186/1471-2105-15-275
Axtell MJ, Meyers BC (2018) Revisiting criteria for plant microRNA annotation in the era of big data. Plant Cell 30:272–284. https://doi.org/10.1105/tpc.17.00851
Axtell MJ, Snyder JA, Bartel DP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19:1750–1769. https://doi.org/10.1105/tpc.107.051706
Babiarz JE, Ruby JG, Wang Y, Bartel DP, Blelloch R (2008) Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessorindependent, dicer-dependent small RNAs. Genes Dev 22:2773–2785. https://doi.org/10.1101/gad.1705308
Banerjee A, Roychoudhury A (2017) Epigenetic regulation during salinity and drought stress in plants: histone modifications and DNA methylation. Plant Gene 11:199–204. https://doi.org/10.1016/j.plgene.2017.05.011
Baras AS, Mitchell CJ, Myers JR, Gupta S, Weng LC, Ashton JM, Cornish TC, Pandey A, Halushka MK (2015) MiRge-a multiplexed method of processing small RNA-Seq data to determine MicroRNA entropy. PLoS One 10:e0143066. https://doi.org/10.1371/journal.pone.0143066
Barrangou R, Birmingham A, Wiemann S, Beijersbergen RL, Hornung V, Smith AV (2015) Advances in CRISPR-Cas9 genome engineering: lessons learned from RNA interference. Nucleic Acids Res 43:3407–3419. https://doi.org/10.1093/nar/gkv226
Barrera-Figueroa B, Gao L, Diop N, Wu Z, Ehlers J, Roberts P, Close T, Zhu J-K, Liu R (2011) Identification and comparative analysis of drought-associated microRNAs in two cowpea genotypes. BMC Plant Biol 11:127. https://doi.org/10.1186/1471-2229-11-127
Barrera-Figueroa BE, Gao L, Wu Z, Zhou X, Zhu J, Jin H, Liu R, Zhu JK (2012) High throughput sequencing reveals novel and abiotic stress-regulated microRNAs in the inflorescences of rice. BMC Plant Biol 12:132. https://doi.org/10.1186/1471-2229-12-132
Bartel D (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297. https://doi.org/10.1016/s0092-8674(04)00045-5
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. https://doi.org/10.3389/fpls.2015.01001
Bhattacharya A, Ziebarth JD, Cui Y (2014) PolymiRTS database 3.0: linking polymorphisms in microRNAs and their target sites with human diseases and biological pathways. Nucleic Acids Res 42(D1):D86–D91. https://doi.org/10.1093/nar/gkt1028
Bonnet E, He Y, Billiau K, Vande PY (2010) TAPIR, a web server for the prediction of plant microRNA targets, including target mimics. Bioinformatics 26:1566–1568. https://doi.org/10.1093/bioinformatics/btq233
Bottino MC, Rosario S, Grativol C, Thiebaut F, Rojas CA, Farrineli L et al (2013) High-throughput sequencing of smallRNA transcriptome reveals salt stress regulated microRNAs in sugarcane. PLoS One 8:e59423. https://doi.org/10.1371/journal.pone.0059423
Brown JW, Marshall DF, Echeverria M (2008) Intronic noncoding RNAs and splicing. Trends Plant Sci 13:335–342. https://doi.org/10.1016/j.tplants.2008.04.010
Buchner P, Takahashi H, Hawkesford MJ (2004) Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J Exp Bot 55:1765–1773. https://doi.org/10.1093/jxb/erh206
Cao X, Aufsatz W, Zilberman D, Mette MF, Huang MS, Matzke M, Jacobsen SE (2003) Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr Biol 13(24):2212–2217. https://doi.org/10.1016/j.cub.2003.11.052
Chak LL, Mohammed J, Lai EC, Tucker-Kellogg G, Okamura K (2015) A deeply conserved, noncanonical miRNA hosted by ribosomal DNA. RNA 21:375–384. https://doi.org/10.1261/rna.049098.114
Chang H, Yi B, Ma R, Zhang X, Zhao H, Xi Y (2016) CRISPR/cas9, a novel genomic tool to knock down microRNA in vitro and in vivo. Sci Rep 6:22312. https://doi.org/10.1038/srep22312
Chen X, Zhang Z, Liu D, Zhang K, Li A, Mao L (2010) SQUAMOSA promoter-binding protein-like transcription factors: star players for plant growth and development. J Integr Plant Biol 52:946–951. https://doi.org/10.1111/j.1744-7909.2010.00987.x
Chen L, Heikkinen L, Wang CL, Yang Y, Knott KE, Wong G (2018) miRToolsGallery: a microRNA bioinformatics resources database portal. Database 2018:bay004. https://doi.org/10.1093/database/bay004
Chou CH, Shrestha S, Yang CD, Chang NW, Lin YL, Liao KW, Huang WC, Sun TH, Tu SJ, Lee WH, Chiew MY et al (2018) miRTarBase update 2018: a resource for experimentally validated microRNA-target interactions. Nucleic Acids Res 46(D1):D296–D302. https://doi.org/10.1093/nar/gkx1067
Cui N, Sun X, Sun M, Jia B, Duanmu H, Lv D et al (2015) Overexpression of OsmiR156k leads to reduced tolerance to cold stress in rice (Oryza sativa). Mol Breed 35:214. https://doi.org/10.1007/s11032-015-0402-6
De Paola D, Zuluaga DL, Sonnante G (2016) The miRNAome of durum wheat: isolation and characterisation of conserved and novel microRNAs and their target genes. BMC Genomics 17:505. https://doi.org/10.1186/s12864-016-2838-4
Deng P, Wang L, Cui L, Feng K, Liu F, Du X et al (2015) Global identification of microRNAs and their targets in barley under salinity stress. PLoS One 10:e0137990. https://doi.org/10.1371/journal.pone.0137990
Delatte B, Fuks F (2013) TET proteins: on the frenetic hunt for new cytosine modifications. Brief Funct Genom 12:191–204. https://doi.org/10.1093/bfgp/elt010
Diaz-Vivancos P, Faize M, Barba-Espin G, Faize L, Petri C, Antonio Hernandez J, Burgos L (2013) Ectopic expression of cytosolic superoxide dismutase and ascorbate peroxidase leads to salt stress tolerance in transgenic plums. Plant Biotechnol J 11:976–985. https://doi.org/10.1111/pbi.12090
Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103:29–38. https://doi.org/10.1093/aob/mcn205
Dong Z, Han MH, Fedoroff N (2008) The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proc Natl Acad Sci 105:9970–9975. https://doi.org/10.1073/pnas.0803356105
Eamens AL, Agius C, Smith NA, Waterhouse PM, Wang MB (2011) Efficient silencing of endogenous microRNAs using artificial microRNAs in Arabidopsis thaliana. Mol Plant 4:157–170. https://doi.org/10.1093/mp/ssq061
Ebert MS, Neilson JR, Sharp PA (2007) MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 4:721. https://doi.org/10.1038/nmeth1079
Eldem V, Çelikkol Akçay U, Ozhuner E, Bakır 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. https://doi.org/10.1371/journal.pone.0050298
Ender C, Krek A, Friedländer MR, Beitzinger M, Weinmann L, Chen W, Pfeffer S, Rajewsky N, Meister G (2008) A human snoRNA with microRNA-like functions. Mol Cell 32:519–528. https://doi.org/10.1016/j.molcel.2008.10.017
Fahad S, Nie L, Chen Y, Wu C, Xiong D, Saud S, Hongyan L, Cui K, Huang J (2015) Crop plant hormones and environmental stress. Sustain Agri Rev 15:371–400. https://doi.org/10.1007/978-3-319-09132-7_10
Fahlgren N, Hill ST, Carrington JC, Carbonell A (2016) P-SAMS: a web site for plant artificial microRNA and synthetic trans-acting small interfering RNA design. Bioinformatics 32:157–158. https://doi.org/10.1093/bioinformatics/btv534
Fang Y, Xie K, Xiong L (2014) Conserved miR164-targeted NAC genes negatively regulate drought resistance in rice. J Exp Bot 65:2119–2135. https://doi.org/10.1093/jxb/eru072
Ferdous J, Sanchez-Ferrero JC, Langridge P, Milne L, Chowdhury J, Brien C, Tricker PJ (2017) Drought-inducible expression of Hv-miR827 enhances drought tolerance in transgenic barley. Funct Integr Genomics 17(2–3):279–292. https://doi.org/10.1007/s10142-016-0526-8
Fernandez J-E (2014) Understanding olive adaptation to abiotic stresses as a tool to increase crop performance. Env Exp Bot 103:158–179. https://doi.org/10.1016/j.envexpbot.2013.12.003
Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, García JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037. https://doi.org/10.1038/ng2079
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. https://doi.org/10.1007/s12033-011-9387-5
Fu C, Sunkar R, Zhou C et al (2012) Overexpression of miR156 in switchgrass (Panicum virgatum L.) results in various morphological alterations and leads to improved biomass production. Plant Biotechnol J 10(4):443–452. https://doi.org/10.1111/j.1467-7652.2011.00677.x
Ganesan G, Sankararamasubramanian HM, Harikrishnan M, Ashwin G, Parida A (2012) A MYB transcription factor from the grey mangrove is induced by stress and confers NaCl tolerance in tobacco. J Exp Bot 63:4549–4561. https://doi.org/10.1093/jxb/ERS135
Gao G, Li J, Li H, Li F, Xu K, Yan G, Chen B, Qiao J, Wu X (2014) Comparison of the heat stress induced variations in DNA methylation between heattolerant and heat-sensitive rapeseed seedlings. Breed Sci 64:125–133. https://doi.org/10.1270/jsbbs.64.125
Gao P, Bai X, Yang L, Lv D, Li Y, Cai H, Ji W, Guo D, Zhu Y (2010) Over-expression of Osa-MIR396c decreases salt and alkali stress tolerance. Planta 231:991–1001. https://doi.org/10.1007/s00425-010-1104-2
Gao P, Bai X, Yang L, Lv D, Pan X, Li Y, Cai H, Ji W, Chen Q, Zhu Y (2011) Osa-MIR393: a salinity- and alkaline stress-related microRNA gene. Mol Biol Rep 38:237–242. https://doi.org/10.1007/s11033-010-0100-8
Gao S, Yang L, Zeng HQ, Zhou ZS, Yang ZM, Li H, Sun D, Xie F, Zhang B (2016) A cotton miRNA is involved in regulation of plant response to salt stress. Sci Rep 4:6122. https://doi.org/10.1038/srep19736
Gentile A, Dias LI, Mattos RS, Ferreira TH, Menossi M (2015) MicroRNAs and drought responses in sugarcane. Front Plant Sci 6:58. https://doi.org/10.3389/fpls.2015.00058
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. https://doi.org/10.1073/pnas.0709559105
Goel S, Goswami K, Pandey VK, Pandey M, Sanan-Mishra N (2019) Identification of microRNA-target modules from rice variety Pusa Basmati-1 under high temperature and salt stress. Funct Integr Genomics 24:1–22. https://doi.org/10.1007/s10142-019-00673-4
Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151. https://doi.org/10.3389/fpls.2014.00151
Gong B, Li X, VandenLangenberg KM, Wen D, Sun S, Wei M, Li Y, Yang F, Shi Q, Wang X (2014) Overexpression of S-adenosyl-lmethionine synthetase increased tomato tolerance to alkali stress through polyamine metabolism. Plant Biotechnol J 12:694–708. https://doi.org/10.1111/pbi.12173
Großkinsky DK, Svensgaard J, Christensen S, Roitsch T (2015) Plant phenomics and the need for physiological phenotyping across scales to narrow the genotype-to-phenotype knowledge gap. J Exp Bot 66:5429–5440. https://doi.org/10.1093/jxb/erv345
Gu Z, Huang C, Li F, Zhou X (2014) A versatile system for functional analysis of genes and microRNAs in cotton. Plant Biotechnol J 12:638–649. https://doi.org/10.1111/pbi.12169
Guan Q, Lu X, Zeng H, Zhang Y, Zhu J (2013) Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant J 74:840–851. https://doi.org/10.1111/tpj.12169
Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17:1376–1386. https://doi.org/10.1105/tpc.105.030841
Gupta PK (2015) MicroRNAs and target mimics for crop improvement. Curr Sci 108:1624–1633
Gurjar AKS, Panwar AS, Gupta R, Mantri SS (2016) PmiRExAt: plant miRNA expression atlas database and web applications. Database 2016:baw060. https://doi.org/10.1093/database/baw060
Hackenberg M, Gustafson P, Langridge P, Shi B-J (2015) Differential expression of microRNAs and other small RNAs in barley between water and drought conditions. Plant Biotechnol J 13:2–13. https://doi.org/10.1111/pbi.12220
Haffner MC, Chaux A, Meeker AK, Esopi DM, Gerber J, Pellakuru LG, Toubaji A, Argani P, Iacobuzio-Donahue C, Nelson WG, Netto GJ (2011) Global 5-hydroxymethylcytosine content is significantly reduced in tissue stem/progenitor cell compartments and in human cancers. Oncotarget 2:627–637. https://doi.org/10.18632/oncotarget.316
Hajyzadeh M, Turktas M, Khawar KM, Unver T (2015) miR408 overexpression causes increased drought tolerance in chickpea. Gene 555:186–193. https://doi.org/10.1016/j.gene.2014.11.002
Iwakawa H-O, Tomari Y (2013) Molecular insights into microRNA mediated translational repression in plants. Mol Cell 52:591–601. https://doi.org/10.1016/j.molcel.2013.10.033
Jang H, Shin H, Eichman BF, Huh JH (2014) Excision of 5-hydroxymethylcytosine by DEMETER family DNA glycosylases. Biochem Biophys Res Commun 446:1067–1072. https://doi.org/10.1016/j.bbrc.2014.03.060
Jean Finnegan E, Dennis ES (1993) Isolation and identification by sequence homology of a putative cytosine methyltransferase from Arabidopsis thaliana. Nucleic Acids Res 21(10):2383–2388. https://doi.org/10.1093/nar/21.10.2383
Jeong DH, Park S, Zhai J, Gurazada SG, 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. https://doi.org/10.1105/tpc.111.089045
Jia X, Wang W-X, Ren L, Chen Q-J, Mendu V, Willcut B, Dinkins R, Tang X, Tang G (2009) Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Mol Biol 71:51–59. https://doi.org/10.1007/s11103-009-9508-8
Jiang X, Zhang C, Lu P, Jiang G, Liu X, Dai F, Gao J (2014) RhNAC3, a stress- associated NAC transcription factor, has a role in dehydration tolerance through regulating osmotic stress- related genes in rose petals. Plant Biotechnol J 12:38–48. https://doi.org/10.1111/pbi.12114
Jiang L, Tian X, Fu Y, Liao X, Wang G, Chen F (2018) Comparative profiling of microRNAs and their effects on abiotic stress in wild-type and dark green leaf color mutant plants of Anthurium andraeanum ‘Sonate’. Plant Physiol Biochem 132:258–270. https://doi.org/10.1016/j.plaphy.2018.09.008
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821. https://doi.org/10.1126/science.1225829
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799. https://doi.org/10.1016/j.molcel.2004.05.027
Jung HJ, Kang H (2007) Expression and functional analyses of microRNA417 in Arabidopsis thaliana under stress conditions. Plant Physiol Biochem 45:805–811. https://doi.org/10.1016/j.plaphy.2007.07.015
Kantar M, Lucas S, Budak H (2011) miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233:471–484. https://doi.org/10.1007/s00425-010-1309-4
Khare T, Shriram V, Kumar V (2018) RNAi technology: the role in development of abiotic stress-tolerant crops. In: Wani SH (ed) Biochemical. Elsevier, Physiological and Molecular Avenues for Combating Abiotic Stress Tolerance in Plants, pp 117–133
Kim W, Benhamed M, Servet C, Latrasse D, Zhang W, Delarue M, Zhou DX (2009) Histone acetyltransferase GCN5 interferes with the miRNA pathway in Arabidopsis. Cell Res 19:899–909. https://doi.org/10.1038/cr.2009.59
Kim J, Lee H, Jung H, Maruyama K, Suzuki N, Kang H (2010a) Overexpression of microRNA395c or 395e affects differently the seed germination of Arabidopsis thaliana under stress conditions. Planta 232:1447–1454. https://doi.org/10.1007/s00425-010-1267-x
Kim JY, Kwak KJ, Jung HJ, Lee HJ, Kang H (2010b) MicroRNA402 affects seed germination of Arabidopsis thaliana under stress conditions via targeting DEMETER-LIKE Protein3 mRNA. Plant Cell Physiol 51:1079–1083. https://doi.org/10.1093/pcp/pcq072
Kinoshita N, Wang H, Kasahara H, Liu J, Macpherson C, Machida Y, Kamiya Y, Hannah MA, Chua NH (2012) IAA-Ala resistant3, an evolutionarily conserved target of miR167, mediates Arabidopsis root architecture changes during high osmotic stress. Plant Cell 24:3590–3602. https://doi.org/10.1105/tpc.112.097006
Kong WW, Yang ZM (2010) Identification of iron-deficiency responsive microRNA genes and cis-elements in Arabidopsis. Plant Physiol Biochem 48:153–159. https://doi.org/10.1016/j.plaphy.2009.12.008
Kong YM, Elling AA, Chen B, Deng XW (2010) Differential expression of microRNAs in maize inbred and hybrid lines during salt and drought stress. Am J Plant Sci 1:69–76. https://doi.org/10.4236/ajps.2010.12009
Kong X, Zhang M, Xu X, Li X, Li C, Ding Z (2014) System analysis of microRNAs in the development and aluminium stress responses of the maize root system. Plant Biotechnol J 12:1108–1121. https://doi.org/10.1111/pbi.12218
Kozomara A, Griffiths-Jones S (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42:D68–D73. https://doi.org/10.1093/nar/gkt1181
Kriaucionis S, Heintz N (2009) The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324:929–930. https://doi.org/10.1126/science.1169786
Kruszka K, Pacak A, Swida-Barteczka A, 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. https://doi.org/10.1093/jxb/eru353
Kudo Y, Tateishi K, Yamamoto K, Yamamoto S, Asaoka Y, Ijichi H, Nagae G, Yoshida H, Aburatani H, Koike K (2012) Loss of 5-hydroxymethylcytosine is accompanied with malignant cellular transformation. Cancer Sci 103:670–676. https://doi.org/10.1111/j.1349-7006.2012.02213.x
Kulcheski FR, de Oliveira LFV, Molina LG et al (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics 12:307. https://doi.org/10.1186/1471-2164-12-307
Kumar V, Khare T (2014) Individual and additive effects of Na+ and cl− ions on rice under salinity stress. Arch Agron Soil Sci 61:381–395. https://doi.org/10.1080/03650340.2014.936400
Kumar V, Khare T, Shriram V, Wani SH (2017) Plant small RNAs: the essential epigenetic regulators of gene expression for salt-stress responses and tolerance. Plant Cell Rep 26:1–5. https://doi.org/10.1007/s00299-017-2210-4
Kurihara Y, Takashi Y, Watanabe Y (2006) The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA 12:206–212. https://doi.org/10.1261/rna.2146906
Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11(3):204. https://doi.org/10.1038/nrg2719
Li H, Dong Y, Yin H, Wang N, Yang J, Liu X et al (2011a) Characterization of the stress associated microRNAs in Glycine max by deep sequencing. BMC Plant Biol 11:170. https://doi.org/10.1186/1471-2229-11-170
Li BS, Qin YR, Duan H, Yin WL, Xia XL (2011b) Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J Exp Bot 62:3765–3779. https://doi.org/10.1093/jxb/err051
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. https://doi.org/10.1007/s11103-013-0010-y
Li S, Liu J, Liu Z, Li X, Wu F, He Y (2014) HEAT-INDUCED TAS1 TARGET1 mediates thermostolerance via HEAT STRESS TRANSCRIPTION FACTOR A1a-directed pathways in Arabidopsis. Plant Cell 26:1764–1780. https://doi.org/10.1105/tpc.114.124883
Li Y, Li C, Bai L, He C, Yu X (2016a) MicroRNA and target gene responses to salt stress in grafted cucumber seedlings. Acta Physiol Plant 38:42. https://doi.org/10.1007/s11738-016-2070-5
Li W, Wang T, Zhang Y, Li Y (2016b) Overexpression of soybean miR172c confers water deficit and salt tolerance but ABA sensitivity in transgenic Arabidopsis thaliana. J Exp Bot 67:175–194. https://doi.org/10.1093/jxb/erv450
Liang M, Haroldsen V, Cai X, Wu Y (2006) Expression of a putative laccase gene, ZmLAC1, in maize primary roots under stress. Plant Cell Environ 29:746–753. https://doi.org/10.1111/j.1365-3040.2005.01435.x
Lin JS, Lin CC, Lin HH, Chen YC, Jeng ST (2012) MicroR828 regulates lignin and H2O2 accumulation in sweet potato on wounding. New Phytol 196:427–440. https://doi.org/10.1111/j.1469-8137.2012.04277.x
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. https://doi.org/10.1261/rna.895308
Liu X, Yang L, Zhou X, Zhou M, Lu Y, Ma L, Ma H, Zhang Z (2013) Transgenic wheat expressing Thinopyrum intermedium MYB transcription factor TiMYB2R-1 shows enhanced resistance to the take-all disease. J Exp Bot 64:2243–2253. https://doi.org/10.1093/jxb/ert084
Liu Y, Li D, Yan J, Wang K, Luo H, Zhang W (2019) MiR319-mediated ethylene biosynthesis, signaling and salt stress response in switchgrass. Plant Biotechnol J. https://doi.org/10.1111/pbi.13154
Long RC, Li MN, Kang JM, Zhang TJ, Sun Y, Yang QC (2015) Small RNA deep sequencing identifies novel and salt-stress-regulated microRNAs from roots of Medicago sativa and Medicago truncatula. Physiol Plant 154:13–27. https://doi.org/10.1111/ppl.12266
López-Galiano MJ, García-Robles I, González-Hernández AI, Camañes G, Vicedo B, Real MD, Rausell C (2019) Expression of miR159 is altered in tomato plants undergoing drought stress. Plants 8(7):201. https://doi.org/10.3390/plants8070201
Lu W, Li J, Liu F, Gu J, GuoC XL, Zhang H, Xiao K (2011) Expression pattern of wheat miRNAs under salinity stress and prediction of salt-inducible miRNAs targets. Front Agri China 5:413–422. https://doi.org/10.1007/s11703-011-1133-z
Lu S, Li Q, Wei H et al (2013) Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc Natl Acad Sci U S A 110:10848–10853. https://doi.org/10.1073/pnas.1308936110
Luo QJ, Mittal A, Jia F, Rock C (2012) An autoregulatory feedback loop involving PAP1 and TAS4 in response to sugars in Arabidopsis. Plant Mol Biol 80:117–129. https://doi.org/10.1007/s11103-011-9778-9
Macovei A, Tuteja N (2012) microRNAs targeting DEAD box helicases are involved in salinity stress response in rice (Oryza sativa L.). BMC Plant Biol 12:183. https://doi.org/10.1186/1471-2229-12-183
Mangrauthia SK, Maliha A, Prathi NB, Marathi B (2017) MicroRNAs: potential target for genome editing in plants for traits improvement. Ind J Plant Physiol 22:530–548. https://doi.org/10.1007/s40502-017-0326-8
Mangrauthia SK, Sailaja B, Pusuluri M, Jena B, Prasanth VV, Agarwal S, Senguttuvel P, Sarla N, Babu VR, Subrahmanyam D, Voleti SR (2018) Deep sequencing of small RNAs reveals ribosomal origin of microRNAs in Oryza sativa and their regulatory role in high temperature. Gene Rep 11:270–278. https://doi.org/10.1016/j.genrep.2018.05.002
Mao X, Zhang H, Qian X, Li A, Zhao G, Jing R (2012) TaNAC2, a NAC type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot 63:2933–2946. https://doi.org/10.1093/jxb/err462
Mao X, Chen S, Li A, Zhai C, Jing R (2014) Novel NAC transcription factor TaNAC67 confers enhanced multi-abiotic stress tolerances in Arabidopsis. PLoS One 9:e84359. https://doi.org/10.1371/journal.pone.0084359
Mastakani FD, Pagheh G, Monfared SR, Shams-Bakhsh M (2018) Identification and expression analysis of a microRNA cluster derived from pre-ribosomal RNA in Papaver somniferum L. and Papaver bracteatum L. PLoS One 13:e0199673. https://doi.org/10.1371/journal.pone.0199673
Meng Y, Shao C (2012) Large-scale identification of mirtrons in Arabidopsis and rice. PLoS One 7:e31163. https://doi.org/10.1371/journal.pone.0031163
Meng Y, Ma X, Chen D, Wu P, Chen M (2010) MicroRNA-mediated signaling involved in plant root development. Biochem Biophys Res Commun 393:345–349. https://doi.org/10.1016/j.bbrc.2010.01.129
Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL et al (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20:3186–3190. https://doi.org/10.1105/tpc.108.064311
Milev I, Yahubyan G, Minkov I, Baev V (2011) miRTour: plant miRNA and target prediction tool. Bioinformation 6:248–249
Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19. https://doi.org/10.1016/j.tplants.2005.11.002
Miyoshi K, Miyoshi T, Siomi H (2010) Many ways to generate microRNA-like small RNAs: non-canonical pathways for microRNA production. Mol Gen Genomics 284:95–103. https://doi.org/10.1007/s00438-010-0556-1
Mondal TK, Ganie SA (2014) Identification and characterization of salt responsive miRNA-SSR markers in rice (Oryza sativa). Gene 535:204–209. https://doi.org/10.1016/j.gene.2013.11.033
Moricová P, Ondřej V, Navrátilová B, Luhová L (2013) Changes of DNA methylation and hydroxymethylation in plant protoplast cultures. Acta Biochim Pol 60:33–36
Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:97–103. https://doi.org/10.1016/j.bbagrm.2011.10.005
Naya L, Paul S, Valdés-López O, Mendoza-Soto AB, Nova-Franco B, Sosa-Valencia G, Reyes JL, Hernández G (2014) Regulation of copper homeostasis and biotic interactions by microRNA 398b in common bean. PLoS One 9:e84416. https://doi.org/10.1371/journal.pone.0084416
Ni Z, Hu Z, Jiang Q, Zhang H (2012) Overexpression of gma-MIR394a confers tolerance to drought in transgenic Arabidopsis thaliana. Biochem Biophys Res Commu 427:330–335. https://doi.org/10.1016/j.bbrc.2012.09.055
Ni Z, Hu Z, Jiang Q, Zhang H (2013) GmNFYA3, a target gene of miR169, is a positive regulator of plant tolerance to drought stress. Plant Mol Biol 82:113–129. https://doi.org/10.1007/s11103-013-0040-5
Noman A, Fahad S, Aqeel M, Ali U, Anwar S, Baloch SK, Zainab M (2017) miRNAs: major modulators for crop growth and development under abiotic stresses. Biotechnol Lett 39(5):685–700. https://doi.org/10.1007/s10529-017-2302-9
Okamura K, Hagen JW, Duan H, Tyler DM, Lai EC (2007) The mirtron pathway generates microRNA-class regulatory RNAs in drosophila. Cell 130:89–100. https://doi.org/10.1016/j.cell.2007.06.028
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. https://doi.org/10.1371/journal.pone.0095800
Pandurangaiah M, Rao GL, Sudhakarbabu O, Nareshkumar A, Kiranmai K, Lokesh U, Thapa G, Sudhakar C (2014) Overexpression of horsegram (Macrotyloma uniflorum lam.Verdc.) NAC transcriptional factor (MuNAC4) in groundnut confers enhanced drought tolerance. Mol Biotechnol 56:758–769. https://doi.org/10.1007/s12033-014-9754-0
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295. https://doi.org/10.1016/j.pbi.2011.02.001
Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18:2368–2379. https://doi.org/10.1101/gad.1231804
Pieczynski M, Marczewski W, Hennig J et al (2013) Down-regulation of CBP80 gene expression as a strategy to engineer a drought-tolerant potato. Plant Biotechnol J 11:459–469. https://doi.org/10.1111/pbi.12032
Raghuram B, Sheikh AH, Sinha AK (2014) Regulation of MAP kinase signaling cascade by microRNAs in Oryza sativa. Plant Signal Behav 9:e29804. https://doi.org/10.4161/psb.29804
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. https://doi.org/10.1101/gad.1476406
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. https://doi.org/10.1111/j.1365-313X.2006.02980.x
Rodriguez-Enriquez J, Dickinson HG, Grant-Downton RT (2011) MicroRNA misregulation: an overlooked factor generating somaclonal variation? Trends Plant Sci 16:242–248. https://doi.org/10.1016/j.tplants.2011.03.002
Ronemus MJ, Galbiati M, Ticknor C, Chen J, Dellaporta SL (1996) Demethylation-induced developmental pleiotropy in Arabidopsis. Science 273(5275):654–657. https://doi.org/10.1126/science.273.5275.654
Rong W, Qi L, Wang A, Ye X, Du L, Liang H, Xin Z, Zhang Z (2014) The ERF transcription factor TaERF3 promotes tolerance to salt and drought stresses in wheat. Plant Biotechnol J 12:468–479. https://doi.org/10.1111/pbi.12153
Ruby JG, Jan CH, Bartel DP (2007) Intronic microRNA precursors that bypass Drosha processing. Nature 448:83–86. https://doi.org/10.1038/nature05983
Saraiya AA, Wang CC (2008) snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog 4:e1000224. https://doi.org/10.1371/journal.ppat.1000224
Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133. https://doi.org/10.1105/tpc.105.039834
Shriram V, Kumar V, Devarumath RM, Khare T, Wani SH (2016) MicroRNAs as potent targets for abiotic stress tolerance in plants. Front Plant Sci 7:817. https://doi.org/10.3389/fpls.2016.00817
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 Genomics 14:233. https://doi.org/10.1186/1471-2164-14-233
Son DJ, Kumar S, Takabe W, Kim CW, Ni CW, Alberts-Grill N, Jang IH, Kim S, Kim W, Kang SW, Baker AH (2013) The atypical mechanosensitive microRNA-712 derived from pre-ribosomal RNA induces endothelial inflammation and atherosclerosis. Nat Commun 4:3000. https://doi.org/10.1038/ncomms4000
Stief A, Altmann S, Hoffmann K, Pant BD, Scheible WR, Bäurle I (2014) Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell 26:1792–1807. https://doi.org/10.1105/tpc.114.123851
Stroud H, Do T, Du J, Zhong X, Feng S, Johnson L, Patel DJ, Jacobsen SE (2014) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol 21(1):64. https://doi.org/10.1038/nsmb.2735
Sun X, Dong B, Yin L, Zhang R, Du W, Liu D, Shi N, Li A, Liang Y, Mao L (2013) PMTED: a plant microRNA target expression database. BMC Bioinformatics 14:174. https://doi.org/10.1186/1471-2105-14-174
Sun X, Xu L, Wang Y, Yu R, Zhu X, Luo X, Gong Y, Wang R, Limera C, Zhang K, Liu L (2015) 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. https://doi.org/10.1186/s12864-015-1416-5
Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203:32–43. https://doi.org/10.1111/nph.12797
Swapna M, Kumar S (2017) MicroRNAs and their regulatory role in sugarcane. Front Plant Sci 8:997. https://doi.org/10.3389/fpls.2017.00997
Szczesniak MW, Makalowska I (2014) miRNEST 2.0: a database of plant and animal microRNAs. Nucleic Acids Res 42:D74–D77. https://doi.org/10.1093/nar/gkt1156
Taft RJ, Glazov EA, Lassmann T, Hayashizaki Y, Carninci P, Mattick JS (2009) Small RNAs derived from snoRNAs. RNA 15:1233–1240. https://doi.org/10.1261/rna.1528909
Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, Rao A (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324:930–935. https://doi.org/10.1126/science.1170116
Tamirisa S, Vudem DR, Khareedu VR (2014) Overexpression of pigeonpea stress-induced cold and drought regulatory gene (CcCDR) confers drought, salt, and cold tolerance in Arabidopsis. J Exp Bot 65:4769–4781. https://doi.org/10.1093/jxb/eru224
Tang G, Tang X (2013) Short tandem target mimic: a long journey to the engineered molecular landmine for selective destruction/blockage of microRNAs in plants and animals. J Genet Genomics 40:291–296. https://doi.org/10.1016/j.jgg.2013.02.004
Tang J, Chu C (2017) MicroRNAs in crop improvement: fine-tuners for complex traits. Nat Plants 3:17077. https://doi.org/10.1038/nplants.2017.77
Tang G, Yan J, Gu Y, Qiao M, Fan R, Mao Y, Tang X (2012) Construction of short tandem target mimic (STTM) to block the functions of plant and animal microRNAs. Methods 58:118–125. https://doi.org/10.1016/j.ymeth.2012.10.006
Teotia S, Tang G (2017) Silencing of stress-regulated miRNAs in plants by short tandem target mimic (STTM) approach. In: Sunkar R (ed) Plant stress tolerance, Methods in molecular biology, vol 1631. Humana Press, New York, pp 337–348. https://doi.org/10.1007/978-1-4939-7136-7_22
Terragni J, Bitinaite J, Zheng Y, Pradhan S (2012) Biochemical characterization of recombinant β-glucosyltransferase and analysis of global 5-hydroxymethylcytosine in unique genomes. Biochemistry 51:1009–1019. https://doi.org/10.1021/bi2014739
Trindade I, Capitão C, Dalmay T, Fevereiro M, Santos DM (2010) miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula. Planta 231:705–716. https://doi.org/10.1007/s00425-009-1078-0
Trumbo JL, Zhang B, Stewart CN (2015) Manipulating microRNAs for improved biomass and biofuels from plant feedstocks. Plant Biotechnol J 13(3):337–354. https://doi.org/10.1111/pbi.12319
Van Dijk K, Ding Y, Malkaram S, Riethoven JJ, Liu R, Yang J, Laczko P, Chen H, Xia Y, Ladunga I, Avramova Z (2010) Dynamic changes in genomewide histone H3 lysine 4 methylation patterns in response to dehydration stress in Arabidopsis thaliana. BMC Plant Biol 10:238. https://doi.org/10.1186/1471-2229-10-238
Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, Mallory AC, Hilbert JL, Bartel DP, Crété P (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16:69–79. https://doi.org/10.1016/j.molcel.2004.09.028
Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687. https://doi.org/10.1016/j.cell.2009.01.046
Voytas DF (2013) Plant genome engineering with sequence-specific nucleases. Annu Rev Plant Biol 64:327–350. https://doi.org/10.1146/annurev-arplant-042811-105552
Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749. https://doi.org/10.1016/j.cell.2009.06.014
Wang TZ, Chen L, Zhao MG, Tian QY, Zhang WH (2011) Identification of drought-responsive microRNAs in Medicago truncatula by genome wide high-throughput sequencing. BMC Genomics 12:367. https://doi.org/10.1186/1471-2164-12-367
Wang Y, Sun F, Cao H, Peng H, Ni Z, Sun Q, Yao Y (2012) TamiR159 directed wheat TaGAMYB cleavage and its involvement in another development and heat response. PLoS One 7:e48445. https://doi.org/10.1371/journal.pone.0048445
Wang M, Wang Q, Zhang B (2013) Response of miRNAs and their targets to salt and drought stresses in cotton (Gossypium hirsutum L.). Gene 530:26–32. https://doi.org/10.1016/j.gene.2013.08.009
Wang B, Sun YF, Song N, Wei JP, Wang XJ, Feng H et al (2014) MicroRNAs involving in cold, wounding and salt stresses in Triticum aestivum L. Plant Physiol Biochem 80:90–96. https://doi.org/10.1016/j.plaphy.2014.03.020
Wang XL, Song SH, Wu YS, Li YL, Chen TT, Huang ZY, Liu S, Dunwell TL, Pfeifer GP, Dunwell JM, Wamaedeesa R (2015) Genome-wide mapping of 5-hydroxymethylcytosine in three rice cultivars reveals its preferential localization in transcriptionally silent transposable element genes. J Exp Bot 66:6651–6663. https://doi.org/10.1093/jxb/erv372
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. https://doi.org/10.1086/605122
Wendte JM, Pikaard CS (2017) The RNAs of RNA-directed DNA methylation. Biochim Biophys Acta 1860(1):140–148. https://doi.org/10.1016/j.bbagrm.2016.08.004
Winter J, Diederichs S (2011) Argonaute proteins regulate microRNA stability. RNA Biol 8:1149–1157. https://doi.org/10.4161/rna.8.6.17665
Winter J, Jung S, Keller S, Gregory RI, Diederichs S (2009) Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 11:228. https://doi.org/10.1038/ncb0309-228
Xia K, Wang R, Ou X, Fang Z, Tian C, Duan J et al (2012) OsTIR1 and OsAFB2 down-regulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS One 7:e30039. https://doi.org/10.1371/journal.pone.0030039
Xie F, Stewart CN, Taki FA, He Q, Liu H, Zhang B (2014) High throughput deep sequencing shows that microRNAs play important roles in switchgrass responses to drought and salinity stress. Plant Biotechnol J 12:354–366. https://doi.org/10.1111/pbi.12142
Xie FL, Jones DC, Wang QL, Sun RR, Zhang BH (2015a) Small RNA sequencing identifies miRNA roles in ovule and fiber development. Plant Biotechnol J 13(3):355–369. https://doi.org/10.1111/pbi.12296
Xie F, Wang Q, Sun R, Zhang B (2015b) Deep sequencing reveals important roles of microRNAs in response to drought and salinity stress in cotton. J Exp Bot 66:789–804. https://doi.org/10.1093/jxb/eru437
Xie FL, Wang QL, Zhang BH (2015c) Global microRNA modification in cotton (Gossypium hirsutum L.). Plant Biotechnol J 13(4):492–500. https://doi.org/10.1111/pbi.12271
Xin M, Wang Y, Yao Y, Song N, Hu Z, Qin D et al (2011) Identification and characterization of wheat long non-protein coding RNAs responsive to powdery mildew infection and heat stress by using microarray analysis and SBS sequencing. BMC Plant Biol 11:61. https://doi.org/10.1186/1471-2229-11-61
Xu Q, He Q, Li S, Tian Z (2014a) Molecular characterization of StNAC2 in potato and its overexpression confers drought and salt tolerance. Acta Physiol Plant 36:1841–1851. https://doi.org/10.1007/s11738-014-1558-0
Xu MY, Zhang L, Li WW, Hu XL, Wang M-B, Fan YL, Zhang CY, Wang L (2014b) Stress-induced early flowering is mediated by miR169 in Arabidopsis thaliana. J Exp Bot 65:89–101. https://doi.org/10.1093/jxb/ert353
Xu J, Hou Q-M, Khare T, Verma SK, Kumar V (2019) Exploring miRNAs for developing climate-resilient crops: a perspective review. Sci Total Environ 653:91–104. https://doi.org/10.1016/j.scitotenv.2018.10.340
Yan J, Gu Y, Jia X, Kang W, Pan S, Tang X, Chen X, Tang G (2012) Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis. Plant Cell 24:415–427. https://doi.org/10.1105/tpc.111.094144
Yang JS, Lai EC (2011) Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol Cell 43:892–903. https://doi.org/10.1016/j.molcel.2011.07.024
Yang C, Li D, Mao D, Liu XUE, Ji C, Li X, Zhao X, Cheng Z, Chen C, Zhu L (2013) Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.). Plant Cell Environ 36:2207–2218. https://doi.org/10.1111/pce.12130
Yang B, Tang J, Yu Z, Khare T, Srivastav A, Datir S, Kumar V (2019a) Light stress responses and prospects for engineering light stress tolerance in crop plants. J Plant Growth Regul. https://doi.org/10.1007/s00344-019-09951-8
Yang T, Wang Y, Teotia S, Wang Z, Shi C, Sun H, Gu Y, Zhang Z, Tang G (2019b) The interaction between miR160 and miR165/166 in the control of leaf development and drought tolerance in Arabidopsis. Sci Rep 9:2832. https://doi.org/10.1038/s41598-019-39397-7
Yao Q, Song CX, He C, Kumaran D, Dunn JJ (2012) Heterologous expression and purification of Arabidopsis thaliana VIM1 protein: in vitro evidence for its inability to recognize hydroxymethylcytosine, a rare base in Arabidopsis DNA. Protein Expr Purif 83:104–111. https://doi.org/10.1016/j.pep.2012.03.003
Yi X, Zhenhai Z, Yi L, Xu W, Zhen S (2015) PNRD: a plant non-coding RNA database. Nucleic Acids Res 43:D982–D989. https://doi.org/10.1093/nar/gku1162
Yin Z, Li Y, Yu J, Liu Y, Li C, Han X, Shen F (2012) Difference in miRNA expression profiles between two cotton cultivars with distinct salt sensitivity. Mol Biol Rep 39:4961–4970. https://doi.org/10.1007/s11033-011-1292-2
Zafar S, Ashraf MY, Anwar S, Ali Q, Noman A (2016) Yield enhancement in wheat by soil and foliar fertilization of K and Zn under saline environment. Soil Environ 35:46–55
Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, Harmer SL, Zilberman D (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153(1):193–205. https://doi.org/10.1016/j.cell.2013.02.033
Zhai J, Zhao Y, Simon SA et al (2013) Plant microRNAs display differential 3′ truncation and tailing modifications that are ARGONAUTE1 dependent and conserved across species. Plant Cell 25:2417–2428. https://doi.org/10.1105/tpc.113.114603
Zhang ZJ (2014) Artificial trans-acting small interfering RNA: a tool for plant biology study and crop improvements. Planta 239:1139–1146. https://doi.org/10.1007/s00425-014-2054-x
Zhang B (2015) MicroRNA: a new target for improving plant tolerance to abiotic stress. J Exp Bot 66(7):1749–1761. https://doi.org/10.1093/jxb/erv013
Zhang B, Wang Q (2015) MicroRNA-based biotechnology for plant improvement. J Cell Physiol 230:1–15. https://doi.org/10.1002/jcp.24685
Zhang BH, Pan XP, Wang QL, Cobb GP, Anderson TA (2005) Identification and characterization of new plant microRNAs using EST analysis. Cell Res 15:336–360. https://doi.org/10.1038/sj.cr.7290302
Zhang B, Wang Q, Pan X (2007) MicroRNAs and their regulatory roles in animals and plants. J Cell Physiol 210:279–289. https://doi.org/10.1002/jcp.20869
Zhang Z, Yu J, Li D, Zhang Z, Liu F, Zhou X, Wang T, Ling Y, Su Z (2010) PMRD: plant microRNA database. Nucleic Acids Res 38(suppl_1):D806–D813. https://doi.org/10.1093/nar/gkp818
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. https://doi.org/10.1007/s10529-010-0436-0
Zhang LW, Song JB, Shu XX, Zhang Y, Yang ZM (2013a) miR395 is involved in detoxification of cadmium in Brassica napus. J Hazard Mater 250–251:204–211. https://doi.org/10.1016/j.jhazmat.2013.01.053
Zhang J, Zhang S, Li S, Han S, Wu T, Li X, Qi L (2013b) A genome-wide survey of microRNA truncation and 3′ nucleotide addition events in larch (Larix leptolepis). Planta 237:1047–1056. https://doi.org/10.1007/s00425-012-1823-7
Zhang P, Meng X, Chen H, Liu Y, Xue J, Zhou Y, Chen M (2017) PlantCircNet: a database for plant circRNA–miRNA–mRNA regulatory networks. Database 2017:1. https://doi.org/10.1093/database/bax089
Zhang J, Zhang H, Srivastava AK, Pan Y, Bai J, Fang J, Shi H, Zhu J-K (2018) Knockdown of rice microRNA166 confers drought resistance by causing leaf rolling and altering stem xylem development. Plant Physiol 176:2082–2094. https://doi.org/10.1104/pp.17.01432
Zhao BT, Liang RQ, Ge LF, Li W, Xiao HS, Lin HX, Ruan KC, Jin YX (2007) Identification of drought-induced microRNAs in rice. Biochem Biophys Res Commun 354:585–590. https://doi.org/10.1016/j.bbrc.2007.01.022
Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y (2009) Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 10:1–10. https://doi.org/10.1186/1471-2199-10-29
Zhao M, Ding H, Zhu J-K, Zhang F, Li W-X (2011) Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytol 190:906–915. https://doi.org/10.1111/j.1469-8137.2011.03647.x
Zhao Y, Wen H, Teotia S, Du Y, Zhang J, Li J, Sun H, Tang G, Peng T, Zhao Q (2017) Suppression of microRNA159 impacts multiple agronomic traits in rice (Oryza sativa L.). BMC Plant Biol 17(1):215. https://doi.org/10.1186/s12870-017-1171-7
Zhao J, Yuan S, Zhou M, Yuan N, Li Z, Hu Q, Bethea FG, Liu H, Li S, Luo H (2018) Transgenic creeping bentgrass overexpressing Osa-miR393a exhibits altered plant development and improved multiple stress tolerance. Plant Biotechnol J 17:233–251. https://doi.org/10.1111/pbi.12960
Zhou X, Wang G, Zhang W (2007) UV-B responsive microRNA genes in Arabidopsis thaliana. Mol Syst Biol 3:103–103. https://doi.org/10.1038/msb4100143
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. https://doi.org/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. https://doi.org/10.1104/pp.112.208702
Zhou J, Deng K, Cheng Y, Zhong Z, Tian L, Tang X, Tang A, Zheng X, Zhang T, Qi Y, Zhang Y (2017) CRISPR-Cas9 based genome editing reveals new insights into microRNA function and regulation in rice. Front Plant Sci 8:1598. https://doi.org/10.3389/fpls.2017.01598
Zhu QH, Spriggs A, Matthew L, Fan L, Kennedy G, Gubler F, Helliwell C (2008) A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Res 18:1456–1465. https://doi.org/10.1101/gr.075572.107
Zhuang Y, Zhou XH, Liu J (2014) Conserved miRNAs and their response to salt stress in wild eggplant Solanum linnaeanum roots. Int J Mol Sci 15:839–849. https://doi.org/10.3390/ijms15010839
Acknowledgments
VK acknowledges the support under Star College Scheme of Department of Biotechnology (DBT), Government of India; FIST program of Department of Science and Technology (DST), Government of India implemented at Modern College, Ganeshkhind, Pune; and Extra Mural Research funds (EMR/2016/003896) from the Science and Engineering Research Board (SERB), Government of India.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Wani, S.H., Kumar, V., Khare, T. et al. miRNA applications for engineering abiotic stress tolerance in plants. Biologia 75, 1063–1081 (2020). https://doi.org/10.2478/s11756-019-00397-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11756-019-00397-7