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Plant microRNAs: Recent Advances and Future Challenges

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Abstract

MicroRNAs (miRNAs) are small ∼20–24 nt species of non-coding RNAs that modulate plant gene expression by means of gene silencing through sequence-specific inhibition of target mRNAs. MiRNAs derive from pol-II transcription of non-coding genes that are precisely processed in nuclear Dicing bodies by a microprocessor complex (dicer-like1–serrate–hyponastic leaves 1: DCL1-SE-HYL1), which recognizes stem-loop secondary-structure features of primary precursor miRNA transcripts (pri-miRNA). The proper processing of the pri-miRNAs results in a double-stranded small RNA that will eventually exit the nucleus and be loaded predominantly onto the effector complex Argonaute1 (Ago1). The single-stranded mature miRNA will guide AGO1, leading to cleavage or translational arrest of complementary mRNAs. MiRNA steady-state levels and activity are regulated not only by transcription rate of precursor transcripts, but also by direct degradation mediated by small RNA degrading nuclease1 (SDN1). miRNAs are retailored by 3′ editing through 2-O-methylation, uridylation and adenlylation, involving Hua enhancer1 (HEN1), HEN1 suppressor1 (HESO1) and probably the exosome—a phenomenon that has been elucidated only scarcely to date in Arabidopsis. MiRNA activity is involved not only in plant development, but also in signaling, abiotic stresses such as drought, heat and metal toxicity, pathogen interaction and symbiotic relationship regulation, among others. The engineering of miRNAs is paving the way to next-generation plant biotechnology by means of over-expression of natural miRNAs, generation of artificial microRNAs and inhibition of miRNA activity by target mimicry. This review highlights the importance of miRNAs in plant sciences by describing the latest updates in this research field.

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References

  • Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221

    PubMed  CAS  Google Scholar 

  • Auer C (2011) Small RNAs for crop improvement: applications and considerations for ecological risk assessments. In:  Erdmann VA, Barciszewski J (eds) Non-coding RNAs in plants. Springer, Berlin, pp 461–484

  • Auer C, Frederick R (2009) Crop improvement using small RNAs: applications and predictive ecological risk assessments. Trends Biotechnol 27:644–651

    PubMed  CAS  Google Scholar 

  • Axtell MJ, Bowman JL (2008) Evolution of plant microRNAs and their targets. Trends Plant Sci 13:343–349

    Google Scholar 

  • Axtell MJ, Jan C, Rajagopalan R, Bartel DP (2006) A two-hit trigger for siRNA biogenesis in plants. Cell 127:565–577

    PubMed  CAS  Google Scholar 

  • Balmer D, Mauch-Mani B (2013) Small yet mighty microRNAs in plant-microbe interactions. MicroRNA 2(1):73–80

    CAS  Google Scholar 

  • Bazin J, Khan GA, Combier J-P et al (2013) miR396 affects mycorrhization and root meristem activity in the legume Medicago truncatula. Plant J 74:920–934

    PubMed  CAS  Google Scholar 

  • Bazzini AA, Hopp HE, Beachy RN, Asurmendi S (2007) Infection and coaccumulation of tobacco mosaic virus proteins alter microRNA levels, correlating with symptom and plant development. Proc Natl Acad Sci USA 104:12157–12162

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bergonzi S, Albani MC, Loren V, van Themaat E et al (2013) Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina. Science 340:1094–1097

    PubMed  CAS  Google Scholar 

  • Bologna NG, Schapire AL, Zhai J et al (2013) Multiple RNA recognition patterns during microRNA biogenesis in plants. Genome Res 23:1675–1689

    PubMed  CAS  PubMed Central  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Brousse C, Liu Q, Beauclair L, et al. (2014) A non-canonical plant microRNA target site. Nucleic Acids Res. doi: 10.1093/nar/gku157

  • Burko Y, Shleizer-Burko S, Yanai O et al (2013) A role for APETALA1/fruitfull transcription factors in tomato leaf development. Plant Cell 25:2070–2083

    PubMed  CAS  PubMed Central  Google Scholar 

  • Campo S, Peris-Peris C, Siré C et al (2013) Identification of a novel microRNA (miRNA) from rice that targets an alternatively spliced transcript of the Nramp6 (Natural resistance-associated macrophage protein 6) gene involved in pathogen resistance. New Phytol 199:212–227

    PubMed  CAS  Google Scholar 

  • Carbonell A, Fahlgren N, Garcia-Ruiz H et al (2012) Functional analysis of three Arabidopsis ARGONAUTES using slicer-defective mutants. Plant Cell 24:3613–3629

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cesana M, Daley GQ (2013) Deciphering the rules of ceRNA networks. Proc Natl Acad Sci USA 110:7112–7113

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chaabane S, Liu R, Chinnusamy V et al (2013) STA1, an Arabidopsis pre-mRNA processing factor 6 homolog, is a new player involved in miRNA biogenesis. Nucleic Acids Res 41:1984–1997

    PubMed  PubMed Central  Google Scholar 

  • Chapman EJ, Prokhnevsky AI, Gopinath K et al (2004) Viral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step. Genes Dev 18:1179–1186

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chen X (2012) Small RNAs in development—insights from plants. Curr Opin Genet Dev 22:361–7

    PubMed  PubMed Central  Google Scholar 

  • Chen H-M, Chen L-T, Patel K et al (2010) 22-nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proc Natl Acad Sci USA 107:15269–15274

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chen L, Zhang Y, Ren Y et al (2012) Genome-wide identification of cold-responsive and new microRNAs in Populus tomentosa by high-throughput sequencing. Biochem Biophys Res Commun 417:892–896

    PubMed  CAS  Google Scholar 

  • Chen X, Zen K, Zhang C-Y (2013) Reply to Lack of detectable oral bioavailability of plant microRNAs after feeding in mice. Nat Biotechnol 31:967–969

    PubMed  CAS  Google Scholar 

  • Cho SH, Coruh C, Axtell MJ (2012) miR156 and miR390 regulate tasiRNA accumulation and developmental timing in Physcomitrella patens. Plant Cell 24:4837–4849

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cloonan N, Wani S, Xu Q et al (2011) MicroRNAs and their isomiRs function cooperatively to target common biological pathways. Genome Biol 12:R126

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cuperus J, Carbonell A, Fahlgren NH (2010) Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat Struct Mol Biol 17:997–1003

    PubMed  CAS  PubMed Central  Google Scholar 

  • De Felippes FF, Wang J, Weigel D (2012) MIGS: miRNA-induced gene silencing. Plant J 70:541–547

    PubMed  Google Scholar 

  • De Oliveira LFV, Christoff AP, Margis R (2013) isomiRID: a framework to identify microRNA isoforms. Bioinformatics 29:2521–2523

    PubMed  Google Scholar 

  • Debernardi JM, Rodriguez RE, Mecchia MA, Palatnik JF (2012) Functional specialization of the plant miR396 regulatory network through distinct microRNA-target interactions. PLoS Genet 8:e1002419

    PubMed  CAS  PubMed Central  Google Scholar 

  • Dickinson B, Zhang Y, Petrick JS et al (2013) Lack of detectable oral bioavailability of plant microRNAs after feeding in mice. Nat Biotechnol 31:965–967

    PubMed  CAS  Google Scholar 

  • Ding J, Li D, Ohler U et al (2012) Genome-wide search for miRNA-target interactions in Arabidopsis thaliana with an integrated approach. BMC Genomics 13(Suppl 3):S3

    PubMed  CAS  PubMed Central  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

    PubMed  CAS  Google Scholar 

  • Fischer JJ, Beatty PH, Good AG, Muench DG (2013) Manipulation of microRNA expression to improve nitrogen use efficiency. Plant Sci 210:70–81

    PubMed  CAS  Google Scholar 

  • Franco-zorrilla M, Puga I, Todesco M et al (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037

    PubMed  CAS  Google Scholar 

  • 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 10:443–452

    PubMed  CAS  PubMed Central  Google Scholar 

  • Giacomelli JI, Weigel D, Chan RL, Manavella PA (2012) Role of recently evolved miRNA regulation of sunflower HaWRKY6 in response to temperature damage. New Phytol 195:766–773

    PubMed  CAS  Google Scholar 

  • Guan Q, Lu X, Zeng H et al (2013) Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant J 74:840–851

    PubMed  CAS  Google Scholar 

  • Gupta OP, Sharma P, Gupta RK, Sharma I (2014) MicroRNA mediated regulation of metal toxicity in plants: present status and future perspectives. Plant Mol Biol 84:1–18

    PubMed  CAS  Google Scholar 

  • Hajheidari M, Koncz C, Eick D (2013) Emerging roles for RNA polymerase II CTD in Arabidopsis. Trends Plant Sci 18:633–643

    PubMed  CAS  Google Scholar 

  • Hauser F, Chen W, Deinlein U et al (2013) A genomic-scale artificial microRNA library as a tool to investigate the functionally redundant gene space in Arabidopsis. Plant Cell 25:2848–2863

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ibrahim F, Rymarquis LA, Kim E-J et al (2010) Uridylation of mature miRNAs and siRNAs by the MUT68 nucleotidyltransferase promotes their degradation in Chlamydomonas. Proc Natl Acad Sci USA 107:3906–3911

    PubMed  CAS  PubMed Central  Google Scholar 

  • Iwata Y, Takahashi M, Fedoroff NV, Hamdan SM (2013) Dissecting the interactions of SERRATE with RNA and DICER-LIKE 1 in Arabidopsis microRNA precursor processing. Nucleic Acids Res 41:9129–9140

    PubMed  CAS  PubMed Central  Google Scholar 

  • Jeong D-H, Park S, Zhai J et al (2011) Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23:4185–4207

    PubMed  CAS  PubMed Central  Google Scholar 

  • Jeong D-H, Thatcher SR, Brown RSH et al (2013) Comprehensive investigation of microRNAs enhanced by analysis of sequence variants, expression patterns, ARGONAUTE loading, and target cleavage. Plant Physiol 162:1225–1245

    PubMed  CAS  PubMed Central  Google Scholar 

  • Jia F, Rock CD (2013) MIR846 and MIR842 comprise a cistronic MIRNA pair that is regulated by abscisic acid by alternative splicing in roots of Arabidopsis. Plant Mol Biol 81:447–460

    PubMed  CAS  PubMed Central  Google Scholar 

  • Jin D, Wang Y, Zhao Y, Chen M (2013) MicroRNAs and their cross-talks in plant development. J Genet Genomics 40:161–70

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Källman T, Chen J, Gyllenstrand N, Lagercrantz U (2013) A significant fraction of 21-nucleotide small RNA originates from phased degradation of resistance genes in several perennial species. Plant Physiol 162:741–754

    PubMed  PubMed Central  Google Scholar 

  • Kettles GJ, Drurey C, Schoonbeek H et al (2013) Resistance of Arabidopsis thaliana to the green peach aphid, Myzus persicae, involves camalexin and is regulated by microRNAs. New Phytol 198:1178–1190

    PubMed  CAS  PubMed Central  Google Scholar 

  • Knauer S, Holt AL, Rubio-Somoza I et al (2013) A protodermal miR394 signal defines a region of stem cell competence in the Arabidopsis shoot meristem. Dev Cell 24:125–132

    PubMed  CAS  Google Scholar 

  • Lafforgue G, Martínez F, Niu Q-W et al (2013) Improving the effectiveness of artificial microRNA (amiR)-mediated resistance against Turnip mosaic virus by combining two amiRs or by targeting highly conserved viral genomic regions. J Virol 87:8254–8256

    PubMed  CAS  PubMed Central  Google Scholar 

  • Li F, Pignatta D, Bendix C et al (2012a) MicroRNA regulation of plant innate immune receptors. Proc Natl Acad Sci USA 109:1790–1795

    PubMed  CAS  PubMed Central  Google Scholar 

  • Li S, Yang X, Wu F, He Y (2012b) HYL1 controls the miR156-mediated juvenile phase of vegetative growth. J Exp Bot 63:2787–98

    PubMed  CAS  PubMed Central  Google Scholar 

  • Li J-F, Chung HS, Niu Y et al (2013a) Comprehensive protein-based artificial microRNA screens for effective gene silencing in plants. Plant Cell 25:1507–1522

    PubMed  CAS  PubMed Central  Google Scholar 

  • Li S, Liu L, Zhuang X et al (2013b) MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153:562–574

    PubMed  CAS  PubMed Central  Google Scholar 

  • Li X, Bian H, Song D et al (2013c) Flowering time control in ornamental gloxinia (Sinningia speciosa) by manipulation of miR159 expression. Ann Bot 111:791–799

    PubMed  CAS  PubMed Central  Google Scholar 

  • Liang G, He H, Yu D (2012) Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLoS One 7:e48951

    PubMed  CAS  PubMed Central  Google Scholar 

  • Liu C, Axtell MJ, Fedoroff NV (2012) The helicase and RNaseIIIa domains of Arabidopsis Dicer-Like1 modulate catalytic parameters during microRNA biogenesis. Plant Physiol 159:748–758

    PubMed  CAS  PubMed Central  Google Scholar 

  • Liu Q, Yan Q, Liu Y et al (2013) Complementation of HYPONASTIC LEAVES1 by double-strand RNA-binding domains of DICER-LIKE1 in nuclear dicing bodies. Plant Physiol 163:108–117

    PubMed  CAS  PubMed Central  Google Scholar 

  • Liu Q, Wang F, Axtell MJ (2014) Analysis of complementarity requirements for plant microRNA targeting using a Nicotiana benthamiana quantitative transient assay. Plant Cell. doi: 10.1105/tpc.113.120972

  • Lu S, Sun Y, Chiang VL (2009) Adenylation of plant miRNAs. Nucleic Acids Res 37:1878–1885

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ma C, Lu Y, Bai S et al (2014) Cloning and characterization of miRNAs and their targets, including a novel miRNA-targeted NBS-LRR protein class gene in apple (Golden Delicious). Mol Plant 7:218–230

    PubMed  CAS  Google Scholar 

  • Manacorda CA, Mansilla C, Debat HJ et al (2013) Salicylic acid determines differential senescence produced by two Turnip mosaic virus strains involving reactive oxygen species and early transcriptomic changes. Mol Plant Microbe Interact 26:1486–1498

    PubMed  CAS  Google Scholar 

  • Manavella PA, Hagmann J, Ott F et al (2012a) Fast-forward genetics identifies plant CPL phosphatases as regulators of miRNA processing factor HYL1. Cell 151:859–870

    PubMed  CAS  Google Scholar 

  • Manavella PA, Koenig D, Weigel D (2012b) Plant secondary siRNA production determined by microRNA-duplex structure. Proc Natl Acad Sci USA 109:2461–2466

    PubMed  CAS  PubMed Central  Google Scholar 

  • Manavella PA, Koenig D, Rubio-Somoza I et al (2013) Tissue-specific silencing of Arabidopsis SU(VAR)3-9 HOMOLOG8 by miR171a. Plant Physiol 161:805–812

    PubMed  CAS  PubMed Central  Google Scholar 

  • Martínez F, Elena SF, Daròs J-A (2013) Fate of artificial microRNA-mediated resistance to plant viruses in mixed infections. Phytopathology 103:870–876

    PubMed  Google Scholar 

  • McHale M, Eamens AL, Finnegan EJ, Waterhouse PM (2013) A 22-nt artificial microRNA mediates widespread RNA silencing in Arabidopsis. Plant J 76:519–529

    PubMed  CAS  Google Scholar 

  • Mi S, Cai T, Hu Y et al (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133:116–127

    PubMed  CAS  PubMed Central  Google Scholar 

  • Molnár A, Schwach F, Studholme DJ et al (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447:1126–1129

    PubMed  Google Scholar 

  • Neilsen CT, Goodall GJ, Bracken CP (2012) IsomiRs–the overlooked repertoire in the dynamic microRNAome. Trends Genet 28:544–549

    PubMed  CAS  Google Scholar 

  • Niu Q-W, Lin S-S, Reyes JL et al (2006) Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat Biotechnol 24:1420–1428

    PubMed  CAS  Google Scholar 

  • Palatnik JF, Allen E, Wu X, et al. (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263

    Google Scholar 

  • Palukaitis P, Groen SC, Carr JP (2013) The Rumsfeld paradox: some of the things we know that we don’t know about plant virus infection. Curr Opin Plant Biol 16:513–519

    PubMed  CAS  Google Scholar 

  • Park W, Li J, Song R et al (2002) CARPEL FACTORY, a dicer homolog, and HEN1, a novel protein, Act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495

    PubMed  CAS  Google Scholar 

  • Peragine A, Yoshikawa M, Park MY, Poethig RS (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19:2164–2175

    Google Scholar 

  • Pumplin N, Voinnet O (2013) RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat Rev Microbiol 11:745–760

    Google Scholar 

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

    Google Scholar 

  • Ramachandran V, Chen X (2008) Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science 321:490–1492

    Google Scholar 

  • Ren G, Chen X, Yu B (2012a) Uridylation of miRNAs by hen1 suppressor1 in Arabidopsis. Curr Biol 22:695–700

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ren G, Xie M, Dou Y et al (2012b) Regulation of miRNA abundance by RNA binding protein TOUGH in Arabidopsis. Proc Natl Acad Sci USA 109:12817–12821

    PubMed  CAS  PubMed Central  Google Scholar 

  • Rhoades MW, Reinhart BJ, Lim LP et al (2002) Prediction of Plant MicroRNA Targets. Cell 110:513–520

    PubMed  CAS  Google Scholar 

  • Rodrigo G, Elena SF (2013) MicroRNA precursors are not structurally robust but plastic. Genome Biol Evol 5:181–186

    PubMed  PubMed Central  Google Scholar 

  • Rogers K, Chen X (2012) microRNA biogenesis and turnover in plants. Cold Spring Harb Symp Quant Biol 77:183–194

    PubMed  CAS  Google Scholar 

  • Rubio-Somoza I, Weigel D (2011) MicroRNA networks and developmental plasticity in plants. Trends Plant Sci 16:258–264

    PubMed  CAS  Google Scholar 

  • Rubio-Somoza I, Weigel D (2013) Coordination of flower maturation by a regulatory circuit of three microRNAs. PLoS Genet 9:e1003374

    PubMed  CAS  PubMed Central  Google Scholar 

  • Rubio-Somoza I, Weigel D, Franco-Zorilla J-M et al (2011) ceRNAs: miRNA target mimic mimics. Cell 147:1431–1432

    PubMed  CAS  Google Scholar 

  • Sablok G, Milev I, Minkov 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

    PubMed  CAS  Google Scholar 

  • Salmena L, Poliseno L, Tay Y et al (2011) A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146:353–358

    PubMed  CAS  PubMed Central  Google Scholar 

  • Schwab R, Palatnik JF, Riester M et al (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527

    PubMed  CAS  Google Scholar 

  • Shivaprasad PV, Chen H-M, Patel K et al (2012) A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24:859–874

    PubMed  CAS  PubMed Central  Google Scholar 

  • Speth C, Willing E-M, Rausch S et al (2013) RACK1 scaffold proteins influence miRNA abundance in Arabidopsis. Plant J 76:433–445

    PubMed  CAS  Google Scholar 

  • Tang Z, Zhang L, Xu C et al (2012) Uncovering small RNA-mediated responses to cold stress in a wheat thermosensitive genic male-sterile line by deep sequencing. Plant Physiol 159:721–738

    PubMed  CAS  PubMed Central  Google Scholar 

  • Thieme CJ, Schudoma C, May P, Walther D (2012) Give it AGO: The search for miRNA-Argonaute sorting signals in Arabidopsis thaliana indicates a relevance of sequence positions other than the 5′-position alone. Front Plant Sci 3:272

    PubMed  PubMed Central  Google Scholar 

  • Todesco M, Rubio-Somoza I, Paz-Ares J, Weigel D (2010) A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. PLoS Genet 6:e1001031

    PubMed  PubMed Central  Google Scholar 

  • Todesco M, Balasubramanian S, Cao J et al (2012) Natural variation in biogenesis efficiency of individual Arabidopsis thaliana microRNAs. Curr Biol 22:166–170

    PubMed  CAS  Google Scholar 

  • Turner M, Nizampatnam NR, Baron M et al (2013) Ectopic expression of miR160 results in auxin hypersensitivity, cytokinin hyposensitivity, and inhibition of symbiotic nodule development in soybean. Plant Physiol 162:2042–2055

    PubMed  CAS  PubMed Central  Google Scholar 

  • Varallyay E, Havelda Z (2013) Unrelated viral suppressors of RNA silencing mediate the control of ARGONAUTE1 level. Mol Plant Pathol 14:567–575

    PubMed  CAS  Google Scholar 

  • Varallyay E, Valoczi A, Agyi A et al (2010) Plant virus-mediated induction of miR168 is associated with repression of ARGONAUTE1 accumulation. EMBO J 29:3507–3519

    PubMed  CAS  PubMed Central  Google Scholar 

  • Vazquez F, Vaucheret H, Rajagopalan R et al (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16:69–79

    PubMed  CAS  Google Scholar 

  • Wang J, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749

    PubMed  CAS  Google Scholar 

  • Wang L, Song X, Gu L et al (2013) NOT2 proteins promote polymerase II-dependent transcription and interact with multiple MicroRNA biogenesis factors in Arabidopsis. Plant Cell 25:715–727

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wu G, Park MY, Conway SR et al (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–759

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wu H-J, Wang Z-M, Wang M, Wang X-J (2013a) Widespread long noncoding RNAs as endogenous target mimics for microRNAs in plants. Plant Physiol 161:1875–1884

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wu X, Shi Y, Li J et al (2013b) A role for the RNA-binding protein MOS2 in microRNA maturation in Arabidopsis. Cell Res 23:645–657

    PubMed  CAS  PubMed Central  Google Scholar 

  • Xia R, Meyers BC, Liu Z et al (2013) MicroRNA superfamilies descended from miR390 and their roles in secondary small interfering RNA Biogenesis in Eudicots. Plant Cell 25:1555–1572

    PubMed  CAS  PubMed Central  Google Scholar 

  • Xie Z, Allen E, Fahlgren N et al (2005) Expression of Arabidopsis MIRNA genes. Plant Physiol 138:2145–2154

    PubMed  CAS  PubMed Central  Google Scholar 

  • Xing S, Salinas M, Garcia-Molina A et al (2013) SPL8 and miR156-targeted SPL genes redundantly regulate Arabidopsis gynoecium differential patterning. Plant J 75:566–577

    PubMed  CAS  Google Scholar 

  • Xu L, Wang Y, Zhai L et al (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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yan J, Gu Y, Jia X et al (2012a) Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis. Plant Cell 24:415–427

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yan K, Liu P, Wu C-A et al (2012b) Stress-induced alternative splicing provides a mechanism for the regulation of microRNA processing in Arabidopsis thaliana. Mol Cell 48:521–531

    PubMed  CAS  Google Scholar 

  • Yan Z, Hossain MS, Wang J et al (2013) miR172 regulates soybean nodulation. Mol Plant Microbe Interact 26:1371–1377

    PubMed  CAS  Google Scholar 

  • Yang L, Xu M, Koo Y et al (2013) Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C. Elife 2:e00260

    PubMed  PubMed Central  Google Scholar 

  • Yu B, Yang Z, Li J et al (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307:932–935

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang H, Li L (2013) SQUAMOSA promoter binding protein-like7 regulated microRNA408 is required for vegetative development in Arabidopsis. Plant J 74:98–109

    PubMed  CAS  Google Scholar 

  • Zhang L, Hou D, Chen X et al (2011) Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Res 22:107–126

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang J, Zhang S, Li S et al (2013a) A genome-wide survey of microRNA truncation and 3’ nucleotide addition events in larch (Larix leptolepis). Planta 237:1047–1056

    PubMed  CAS  Google Scholar 

  • Zhang Y-C, Yu Y, Wang C-Y et al (2013b) Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat Biotechnol 31:848–852

    PubMed  CAS  Google Scholar 

  • Zhang X-N, Li X, Liu J-H (2014) Identification of conserved and novel cold-responsive microRNAs in trifoliate orange (Poncirus trifoliata (L.) Raf.) using high-throughput sequencing. Plant Mol Biol Report 32:328–341

    CAS  Google Scholar 

  • Zhao M, Tai H, Sun S et al (2012a) Cloning and characterization of maize miRNAs involved in responses to nitrogen deficiency. PLoS One 7:e29669

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zhao Y, Yu Y, Zhai J et al (2012b) The Arabidopsis nucleotidyl transferase HESO1 uridylates unmethylated small RNAs to trigger their degradation. Curr Biol 22:689–694

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zhao X, Zhang H, Li L (2013) Identification and analysis of the proximal promoters of microRNA genes in Arabidopsis. Genomics 101:187–194

    PubMed  CAS  Google Scholar 

  • Zhou Z, Wang Z, Li W et al (2013a) Comprehensive analyses of microRNA gene evolution in paleopolyploid soybean genome. Plant J 76:332–344

    PubMed  CAS  Google Scholar 

  • Zhou C-M, Zhang T-Q, Wang X et al (2013b) Molecular basis of age-dependent vernalization in Cardamine flexuosa. Science 340:1097–1100

    PubMed  CAS  Google Scholar 

  • Zhu H, Zhou Y, Castillo-González C et al (2013) Bidirectional processing of pri-miRNAs with branched terminal loops by Arabidopsis Dicer-like1. Nat Struct Mol Biol 20:1106–1115

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zou Y, Wang Y, Wang L et al (2013) miR172b controls the transition to autotrophic development inhibited by ABA in Arabidopsis. PLoS One 8:e64770

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zvereva AS, Pooggin MM (2012) Silencing and innate immunity in plant defense against viral and non-viral pathogens. Viruses 4:2578–2597

    PubMed  CAS  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the National Program of Plant Protection, Instituto Nacional de Tecnología Agropecuaria (INTA). The authors would like apologize to colleagues whose work could not be fully cited owing to space constraints.

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  1. Instituto de Patología Vegetal, Centro de Investigaciones Agropecuarias (IPAVE – CIAP), Instituto Nacional de Tecnología Agropecuaria (INTA), Camino 60 cds s/n km 5 y ½, 5119, Córdoba, Argentina

    Humberto J. Debat & Daniel A. Ducasse

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  1. Humberto J. Debat
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  2. Daniel A. Ducasse
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Correspondence to Humberto J. Debat.

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Debat, H.J., Ducasse, D.A. Plant microRNAs: Recent Advances and Future Challenges. Plant Mol Biol Rep 32, 1257–1269 (2014). https://doi.org/10.1007/s11105-014-0727-z

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