Biological significance, computational analysis, and applications of plant microRNAs

  • Maria SzwackaEmail author
  • Magdalena Pawełkowicz
  • Agnieszka Skarzyńska
  • Paweł Osipowski
  • Michał Wojcieszek
  • Zbigniew Przybecki
  • Wojciech PląderEmail author


microRNA molecules belong to a class of small non-coding RNAs composed of 21–24 nucleotides and have been identified in most eukaryotes. These small RNA molecules can either transcriptionally or post-transcriptionally regulate expression of their target messenger RNAs. Access to the latest RNA-profiling technologies (e.g. high-throughput sequencing) in combination with computational analysis has contributed to rapid development in the field of miRNA research. Species-specific and highly conserved miRNAs’ control in plants biological processes. Nevertheless, regulatory functions of plant miRNAs have not been still fully understood. Hence, one of the major challenges in plant miRNA research is to find out their regulatory activities that may create an opportunity to develop new strategies for improving crops. This paper provides an overview of the current knowledge concerning the mechanisms related to plant gene regulation via miRNAs. Moreover, it includes an updated overview on the bioinformatic approaches that are available for identification of new miRNAs and their targets. It also includes some specific data on key functions of plant miRNAs to show potential impact of such small RNA molecules on diverse biological processes and their biotechnological significance. Current challenges and future perspectives have also been highlighted.


Plant microRNA Regulatory mechanisms NGS Bioinformatic tools MicroRNA function; microRNA-based GM technology 



We would like to thank Prof. S. Malepszy (Warsaw University of Life Sciences, Poland) for valuable comments concerning this manuscript. This work has been supported by grants from the National Science Center—2013/11/B/NZ9/00814 and 2011/01/B/NZ2/01631.

Author contributions

MS, MP, and WP conception of the work and wrote the paper; ZP critical revision of the article; MP, AS, and PO data collection for preparing of the tables and figures; and MW preparing of the tables and data verification. MP and AS preparing of the figures. All authors commented on the manuscript at all stages.


  1. Achkar NP, Cambiagno DA, Manavella PA (2016) miRNA biogenesis: a dynamic pathway. Trends Plant Sci 21:1034–1044. PubMedCrossRefGoogle Scholar
  2. Addo-Quaye C, Eshoo TW, Bartel DP, Axtell MJ (2008) Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 18:758–762. PubMedPubMedCentralCrossRefGoogle Scholar
  3. Alazem M, Lin N-S (2015) Roles of plant hormones in the regulation of host-virus interactions. Mol Plant Pathol 16:529–540. PubMedCrossRefGoogle Scholar
  4. Allen E, Xie Z, Gustafson AM, Sung G-H, Spatafora JW, Carrington JC (2004) Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat Genet 36:1282–1290. PubMedCrossRefGoogle Scholar
  5. Alptekin B, Budak H (2016) Wheat miRNA ancestors: evident by transcriptome analysis of A, B, and D genome donors. Funct Integr Genom 17:171–187. CrossRefGoogle Scholar
  6. Amiteye S, Corral JM, Vogel H, Sharbel TF (2011) Analysis of conserved microRNAs in floral tissues of sexual and apomictic Boechera species. BMC Genom 12:500. CrossRefGoogle Scholar
  7. 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. PubMedCrossRefGoogle Scholar
  8. Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741. PubMedPubMedCentralCrossRefGoogle Scholar
  9. Axtell MJ (2013) ShortStack: comprehensive annotation and quantification of small RNA genes. RNA 19:740–751. PubMedPubMedCentralCrossRefGoogle Scholar
  10. Axtell MJ, Snyder JA, Bartel DP (2007) Common functions for diverse smallRNAs of land plants. PlantCell 19:1750–1769. CrossRefGoogle Scholar
  11. Axtell MJ, Westholm JO, Lai EC (2011) Vive la différence: biogenesis and evolution of microRNAs in plants and animals. Genome Biol 12:221. PubMedPubMedCentralCrossRefGoogle Scholar
  12. Baldrich P, San Segundo B (2016) MicroRNAs in rice innate immunity. Rice 9:6. PubMedPubMedCentralCrossRefGoogle Scholar
  13. Banks JA (2008) MicroRNA, sex determination and floral meristem determinacy in maize. Genome Biol 9:204. PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297. PubMedCrossRefGoogle Scholar
  15. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233. PubMedPubMedCentralCrossRefGoogle Scholar
  16. Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci USA 102:11928–11933. PubMedCrossRefGoogle Scholar
  17. Bazin J, Khan GA, Combier J-P, Bustos-Sanmamed P, Debernardi JM, Rodriguez R, Sorin C, Palatnik J, Hartman C, Crepsi M, Lelandais-Brière C (2013) miR396 affects mycorrhization and root meristem activity in the legume Medicago truncatula. Plant J 74:920–934PubMedCrossRefGoogle Scholar
  18. Bej S, Basak J (2014) MicroRNAs: the potential biomarkers in plant stress response. Am J Plant Sci 5:748–759. CrossRefGoogle Scholar
  19. Bhalla PL, Singh MB (2006) Molecular control of stem cell maintenance in shoot apical meristem. Plant Cell Rep 25:249–256. PubMedCrossRefGoogle Scholar
  20. Bi F, Meng X, Ma C, Yi G (2015) Identification of miRNAs involved in fruit ripening in Cavendish bananas by deep sequencing. BMC Genom 16:776. CrossRefGoogle Scholar
  21. Bielewicz D, Dolata J, Zielezinski A et al (2012) mirEX: a platform for comparative exploration of plant pri-miRNA expression data. Nucleic Acids Res 40:D191–D197. PubMedCrossRefGoogle Scholar
  22. 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 14:622–628PubMedPubMedCentralCrossRefGoogle Scholar
  23. Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218:683. PubMedCrossRefGoogle Scholar
  24. Borges F, Pereira PA, Slotkin RK et al (2011) MicroRNA activity in the Arabidopsis male germline. J Exp Bot 62:1611–1620. PubMedPubMedCentralCrossRefGoogle Scholar
  25. Boualem A, Laporte P, Jovanovic M et al (2008) MicroRNA166 controls root and nodule development in Medicago truncatula. Plant J 54:876–887. PubMedCrossRefGoogle Scholar
  26. Branscheid A, Marchais A, Schott G et al (2015) SK12 mediates degradation of RISC 5′-cleavage fragments and prevents secondary siRNA production from miRNA targets in Arabidopsis. Nucleic Acids Res 43(22):10975–10988. PubMedPubMedCentralCrossRefGoogle Scholar
  27. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M et al (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320(5880):1185–1190. PubMedCrossRefGoogle Scholar
  28. Carbonell A, Fahlgren N, Garcia-Ruiz H, Gilbert KB, Montgomery TA, Nguyen T, Cuperus JT, Carrington JC (2012) Functional analysis of three Arabidopsis ARGONAUTES using slicer-defective mutants. Plant Cell 2012(9):3613–3629. CrossRefGoogle Scholar
  29. Carbonell A, Takeda A, Fahlgren N et al (2014) New generation of artificial MicroRNA and synthetic trans-acting small interfering RNA vectors for efficient gene silencing in Arabidopsis. Plant Physiol 165:15–29. PubMedPubMedCentralCrossRefGoogle Scholar
  30. Carbonell A, Fahlgren N, Mitchell S et al (2015) Highly specific gene silencing in a monocot species by artificial microRNAs derived from chimeric miRNA precursors. Plant J 82:1061–1075. PubMedPubMedCentralCrossRefGoogle Scholar
  31. Carbonell A, Carrington JC, Daròs J-A (2016) Fast-forward generation of effective artificial small RNAs for enhanced antiviral defense in plants. RNA Dis 3:e1130. PubMedPubMedCentralCrossRefGoogle Scholar
  32. Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136(4):642–655. PubMedPubMedCentralCrossRefGoogle Scholar
  33. Chen X (2004) A MicroRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025. PubMedCrossRefGoogle Scholar
  34. Chen M, Cao Z (2015) Genome-wide expression profiling of microRNAs in poplar upon infection with the foliar rust fungus Melampsora larici-populina. BMC Genom 16:696. CrossRefGoogle Scholar
  35. Chen ZH, Bao ML, Sun YZ et al (2011) Regulation of auxin response by miR393-targeted transport inhibitor response protein 1 is involved in normal development in Arabidopsis. Plant Mol Biol 77:619–629. PubMedCrossRefGoogle Scholar
  36. Chen W, Kong J, Lai T et al (2015) Tuning LeSPL-CNR expression by SlymiR157 affects tomato fruit ripening. Sci Rep 5:7852. PubMedPubMedCentralCrossRefGoogle Scholar
  37. Chien C-H, Chiang-Hsieh Y-F, Chen Y-A et al (2015) AtmiRNET: a web-based resource for reconstructing regulatory networks of Arabidopsis microRNAs. Database 2015:bav042. PubMedPubMedCentralCrossRefGoogle Scholar
  38. Chitwood DH, Nogueira FTS, Howell MD et al (2009) Pattern formation via small RNA mobility. Genes Dev 23:549–554. PubMedPubMedCentralCrossRefGoogle Scholar
  39. Chorostecki U, Moro B, Rojas AML, Debernardi JM, Schapire AL, Notredame C, Palatnik JF (2017) Evolutionary footprints reveal insights into plant microRNA biogenesis. Plant Cell 29(6):1248–1261. PubMedPubMedCentralCrossRefGoogle Scholar
  40. Chuck G, Cigan AM, Saeteurn K, Hake S (2007a) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39:544–549. PubMedCrossRefGoogle Scholar
  41. Chuck G, Meeley R, Irish E et al (2007b) The maize tasselseed4 microRNA controls sex determination and meristem cell fate by targeting Tasselseed6/indeterminate spikelet1. Nat Genet 39:1517–1521. PubMedCrossRefGoogle Scholar
  42. Combier J-P, Frugier F, de Billy F et al (2006) MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev 20:3084–3088. PubMedPubMedCentralCrossRefGoogle Scholar
  43. Conesa A, Madrigal P, Tarazona S et al (2016) A survey of best practices for RNA-seq data analysis. Genome Biol 17:13. PubMedPubMedCentralCrossRefGoogle Scholar
  44. Cui J, You C, Chen X (2017) The evolution of microRNAs in plants. Curr Opin Plant Biol 35:61–67. PubMedCrossRefGoogle Scholar
  45. Cuperus JT, Fahlgren N, Carrington JC (2011) Evolution and functional diversification of MIRNA genes. Plant Cell 23:431–442. PubMedPubMedCentralCrossRefGoogle Scholar
  46. Curaba J, Singh MB, Bhalla PL (2014) miRNAs in the crosstalk between phytohormone signalling pathways. J Exp Bot 65:1425–1438. PubMedCrossRefGoogle Scholar
  47. D’haeseleer K, Den Herder G, Laffont C, Plet J, Mortier V, Lelandais-Brière C, De Bodt S, De Keyser A, Crepsi M, Holsters M, Frugier F, Goormachtig S (2011) Transcriptional and post-transcriptional regulation of a NAC1 transcription factor in Medicago truncatula roots. New Phytol 191:647–661PubMedCrossRefGoogle Scholar
  48. De Luis A, Markmann K, Cognat V, Holt DB, Charpentier M, Parniske M, Stougaard J, Voinnet O (2012) Two microRNAs linked to nodule infection and nitrogen-fixing ability in the legume Lotus japonicus. Plant Physiol 160:2137–2154PubMedPubMedCentralCrossRefGoogle Scholar
  49. Demirci MDS, Baumbach J, Allmer J (2017) On the performance of pre-microrna detection algorithms. Nat Commun 8:330. CrossRefGoogle Scholar
  50. Denancé N, Sánchez-Vallet A, Goffner D, Molina A (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci 4:155. PubMedPubMedCentralCrossRefGoogle Scholar
  51. Dong Q-H, Han J, Yu H-P, Wang C, Zhao M-Z, Liu H et al (2012) Computational identification of MicroRNAs in strawberry expressed sequence tags and validation of their precise sequences by miR-RACE. J Hered 103(2):268–277. PubMedCrossRefGoogle Scholar
  52. Du P, Wu J, Zhang J et al (2011) Viral infection induces expression of novel phased MicroRNAs from conserved cellular MicroRNA precursors. PLoS Pathog 7:e1002176. PubMedPubMedCentralCrossRefGoogle Scholar
  53. Dugas DV, Bartel B (2008) Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol Biol 67:403–417. PubMedCrossRefGoogle Scholar
  54. 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. PubMedCrossRefGoogle Scholar
  55. Eamens AL, Kim KW, Curtin SJ, Waterhouse PM (2012) DRB2 Is Required for MicroRNA biogenesis in Arabidopsis thaliana. PLoS One 7:e35933. PubMedPubMedCentralCrossRefGoogle Scholar
  56. Ebert MS, Neilson JR, Sharp PA (2007) MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 4:721–726. PubMedCrossRefGoogle Scholar
  57. Eulalio A, Rehwinkel J, Stricker M, Huntzinger E, Yang SF, Doerks T, Dorner S, Bork P, Boutors M, Izaurralde E (2007) Target-specific requirements for enhancers of decapping in miRNA-mediated gene silencing. Genes Dev 21(20):2558–2570. PubMedPubMedCentralCrossRefGoogle Scholar
  58. Eulalio A, Huntzinger E, Nishihara T, Rehwinkel J, Fauser M, Izaurralde E (2009) Deadenylation is a widespread effect of miRNA regulation. RNA 15:21–32. PubMedPubMedCentralCrossRefGoogle Scholar
  59. 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. PubMedCrossRefGoogle Scholar
  60. Fang X, Shi Y, Lu X, Chen Z, Qi Y (2015) CMA33/XCT regulates small RNA production through modulating the transcription of Dicer-like genes in Arabidopsis. Mol Plant 8:1227–1236. PubMedCrossRefGoogle Scholar
  61. Fei Q, Zhang Y, Xia R, Meyers BC (2016) Small RNAs add zing to the Zig-Zag-Zig model of plant defenses. MPMI 29:165–169. PubMedCrossRefGoogle Scholar
  62. Felippes FF de, Schneeberger K, Dezulian T et al (2008) Evolution of Arabidopsis thaliana microRNAs from random sequences. RNA 14(12):2455–2459. PubMedCrossRefGoogle Scholar
  63. Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18:265–276. PubMedCrossRefGoogle Scholar
  64. Feng J, Liu S, Wang M et al (2014) Identification of microRNAs and their targets in tomato infected with Cucumber mosaic virus based on deep sequencing. Planta 240:1335–1352. PubMedCrossRefGoogle Scholar
  65. Formey D, Sallet E, Lelandais-Brière C et al (2014) The small RNA diversity from Medicago truncatula roots under biotic interactions evidences the environmental plasticity of the miRNAome. Genome Biol 15:457. PubMedPubMedCentralCrossRefGoogle Scholar
  66. Franco-Zorrilla JM, Valli A, Todesco M et al (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037. PubMedCrossRefGoogle Scholar
  67. Gao C, Ju Z, Cao D et al (2015) MicroRNA profiling analysis throughout tomato fruit development and ripening reveals potential regulatory role of RIN on microRNAs accumulation. Plant Biotechnol J 13:370–382. PubMedCrossRefGoogle Scholar
  68. Giurato G, De Filippo MR, Rinaldi A et al (2013) iMir: an integrated pipeline for high-throughput analysis of small non-coding RNA data obtained by smallRNA-SEq. BMC Bioinform 14:362. CrossRefGoogle Scholar
  69. Grant-Downton R, Rodriguez-Enriquez J (2012) Emerging roles for non-coding RNAs in male reproductive development in flowering plants. Biomolecules 2:608–621. PubMedPubMedCentralCrossRefGoogle Scholar
  70. Grant-Downton R, Hafidh S, Twell D, Dickinson HG (2009a) Small RNA pathways are present and functional in the angiosperm male gametophyte. Mol Plant 2:500–512. PubMedCrossRefGoogle Scholar
  71. Grant-Downton R, Le Trionnaire G, Schmid R et al (2009b) MicroRNA and tasiRNA diversity in mature pollen of Arabidopsis thaliana. BMC Genom 10:643. CrossRefGoogle Scholar
  72. Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu (2010) Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. Physiol Plant 138:226–237. PubMedCrossRefGoogle Scholar
  73. Gui Y, Yan G, Bo S et al (2011) iSNAP: a small RNA-based molecular marker technique. Plant Breed 130:515–520. CrossRefGoogle Scholar
  74. Guleria P, Mahajan M, Bhardwaj J, Yadav SK (2011) Plant small RNAs: biogenesis, mode of action and their roles in abiotic stresses. Genom Proteom Bioinform 9:183–199. CrossRefGoogle Scholar
  75. Gupta PK (2015) MicroRNAs and target mimics for crop improvement. Curr Sci 108:1624–1633Google Scholar
  76. Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C (2009) Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 21:3119–3132. PubMedPubMedCentralCrossRefGoogle Scholar
  77. Han M-H, Goud S, Song L, Fedoroff N (2004) The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc Natl Acad Sci USA 101:1093–1098. PubMedCrossRefGoogle Scholar
  78. Han Y, Luan F, Zhu H, Shao Y, Chen A, Lu C et al (2009) Computational identification of microRNAs and their targets in wheat (Triticum aestivum L.). Sci China Ser C Life Sci 52(11):1091–1100. CrossRefGoogle Scholar
  79. Hewezi T, Howe P, Maier TR, Baum TJ (2008) Arabidopsis small RNAs and their targets during cyst nematode parasitism. Mol Plant-Microbe Interact 21:1622–1634. PubMedCrossRefGoogle Scholar
  80. Hewezi T, Maier TR, Nettleton D, Baum TJ (2012) The Arabidopsis MicroRNA396-GRF1/GRF3 regulatory module acts as a developmental regulator in the reprogramming of root cells during cyst nematode infection. Plant Physiol 159:321–335. PubMedPubMedCentralCrossRefGoogle Scholar
  81. Hobecker KV, Reynoso MA, Bustos-Sanmamed P, Wen J, Mysore KS, Crespi M, Blanco FA, Zanetti ME (2017) The MicroRNA390/TAS3 pathway mediates symbiotic nodulation and lateral root growth. Plant Physiol 174:2469–2486. PubMedPubMedCentralCrossRefGoogle Scholar
  82. Hong Y, Jackson S (2015) Floral induction and flower formation-the role and potential applications of miRNAs. Plant Biotechnol J 13:282–292. PubMedCrossRefGoogle Scholar
  83. Hou Y, Zhai K, Li X, Xue Y, Wang J, Yang P, Cao C, Li H, Cui Y, Bian S (2017) Comparative analysis of fruit ripening-related miRNAs and their targets in blueberry using small RNA and degradome sequencing. Int J Mol Sci 18:2767. PubMedCentralCrossRefGoogle Scholar
  84. Htwe NMPS, Luo Z-Q, Jin L-G et al (2015) Functional marker development of miR1511-InDel and allelic diversity within the genus Glycine. BMC Genom 16:467. CrossRefGoogle Scholar
  85. Huntzinger E, Izaurralde E (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12:99–110. PubMedCrossRefGoogle Scholar
  86. Íñiguez LP, Nova-Franco B, Hernández G (2015) Novel players in the AP2-miR172 regulatory network for common bean nodulation. Plant Signal Behav 10:e1062957. PubMedPubMedCentralCrossRefGoogle Scholar
  87. Ivashuta S, Banks IR, Wiggins BE et al (2011) Regulation of gene expression in plants through miRNA inactivation. PLoS One 6:e21330. PubMedPubMedCentralCrossRefGoogle Scholar
  88. Iwakawa H-O, Tomari Y (2013) Molecular insights into microRNA-mediated translational. Repression in plants. Mol Cell 52:591–601. PubMedCrossRefGoogle Scholar
  89. Jacob Y, Mongkolsiriwatana C, Veley KM, Kim SY, Michaels SD (2007) The nuclear pore protein AtTPR is required for RNA homeostasis, flowering time, and auxin signaling. Plant Physiol 144:1383–1390PubMedPubMedCentralCrossRefGoogle Scholar
  90. Jagadeeswaran G, Saini A, Sunkar R (2009) Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 229:1009–1014. PubMedCrossRefGoogle Scholar
  91. Jha A, Shankar R (2011) Employing machine learning for reliable miRNA target identification in plants. BMC Genom 12:636. CrossRefGoogle Scholar
  92. Jian C, Han R, Chi Q, Wang S, Ma M, Liu X, Zhao H (2017) Virus-based MicroRNA silencing and overexpressing in common wheat (Triticum aestivum L.). Front Plant Sci 8:500. PubMedPubMedCentralCrossRefGoogle Scholar
  93. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799. PubMedCrossRefGoogle Scholar
  94. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53. PubMedCrossRefPubMedCentralGoogle Scholar
  95. Kamthan A, Chaudhuri A, Kamthan M, Datta A (2015) Small RNAs in plants: recent development and application for crop improvement. Front Plant Sci 6:208. PubMedPubMedCentralCrossRefGoogle Scholar
  96. Kant S, Bi Y-M, Rothstein SJ (2011) Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. J Exp Bot 62:1499–1509. PubMedCrossRefGoogle Scholar
  97. Karakülah G, Yücebilgili Kurtoğlu K, Unver T (2016) PeTMbase: a database of plant endogenous target mimics (eTMs). PLoS One 11:e0167698. PubMedPubMedCentralCrossRefGoogle Scholar
  98. Kehr J, Buhtz A (2007) Long distance transport and movement of RNA through the phloem. J Exp Bot 59:85–92. PubMedCrossRefGoogle Scholar
  99. Khaldun ABM, Huang W, Lv H, Liao S, Zeng S, Wang Y (2016) Comparative profiling of miRNAs and Target gene identification in distant-grafting between tomato and lycium (Goji Berry). Front Plant Sci 7:1475. PubMedPubMedCentralCrossRefGoogle Scholar
  100. Khraiwesh B, Ossowski S, Weigel D et al (2008) Specific gene silencing by artificial MicroRNAs in Physcomitrella patens: an alternative to targeted gene knockouts. Plant Physiol 148:684–693. PubMedPubMedCentralCrossRefGoogle Scholar
  101. Khraiwesh B, Arif MA, Seumel GI et al (2010) Transcriptional control of gene expression by MicroRNAs. Cell 140:111–122. PubMedCrossRefGoogle Scholar
  102. 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. PubMedCrossRefGoogle Scholar
  103. Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6:376–385. PubMedCrossRefGoogle Scholar
  104. Kim YJ, Chen X (2011) The plant Mediator and its role in noncoding RNA production. Front Biol (Beijing) 6:125–132. CrossRefGoogle Scholar
  105. Koter MD, Święcicka M, Matuszkiewicz M et al (2018) The miRNAome dynamics during developmental and metabolic reprogramming of tomato root infected with potato cyst nematode. Plant Sci 268:18–29. PubMedCrossRefGoogle Scholar
  106. Kulcheski FR, de Oliveira LF, Molina LG et al (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genom 12:307. CrossRefGoogle Scholar
  107. Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101:12753–12758PubMedCrossRefGoogle Scholar
  108. Lalonde S, Boles E, Hellmann H et al (1999) The dual function of sugar carriers. Transport and sugar sensing. Plant Cell 11:707–726. PubMedPubMedCentralCrossRefGoogle Scholar
  109. Lanet E, Delannoy E, Sormani R et al (2009) Biochemical evidence for translational repression by Arabidopsis microRNAs. Plant Cell 21:1762–1768. PubMedPubMedCentralCrossRefGoogle Scholar
  110. Lee Y-S, Lee D-Y, Cho L-H, An G (2014) Rice miR172 induces flowering by suppressing OsIDS1 and SNB, two AP2 genes that negatively regulate expression of Ehd1 and florigens. Rice 7:31. PubMedPubMedCentralCrossRefGoogle Scholar
  111. Lelandais-Brière C, Naya L, Sallet E et al (2009) Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell 21:2780–2796. PubMedPubMedCentralCrossRefGoogle Scholar
  112. Levin JZ, Yassour M, Adiconis X et al (2010) Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat Methods 7:709–715. PubMedPubMedCentralCrossRefGoogle Scholar
  113. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB (2003) Prediction of mammalian microRNA targets. Cell 115:787–798PubMedCrossRefGoogle Scholar
  114. Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120(1):15–20. PubMedCrossRefGoogle Scholar
  115. Li A, Mao L (2007) Evolution of plant microRNA gene families. Cell Res 17:212–218. PubMedCrossRefGoogle Scholar
  116. Li J, Yang Z, Yu B, Liu J, Chen X (2005) Methylation protects miRNAs and siRNAs from 3′-end uridylation activity in Arabidopsis. Curr Biol 15(16):1501–1507. PubMedPubMedCentralCrossRefGoogle Scholar
  117. Li H, Deng Y, Wu T et al (2010) Misexpression of miR482, miR1512, and miR1515 increases soybean nodulation. Plant Physiol 153:1759–1770. PubMedPubMedCentralCrossRefGoogle Scholar
  118. 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. PubMedCrossRefGoogle Scholar
  119. Li F, Pignatta D, Bendix C et al (2012) MicroRNA regulation of plant innate immune receptors. Proc Natl Acad Sci 109:1790–1795. PubMedCrossRefGoogle Scholar
  120. Li S, Liu L, Zhuang X et al (2013a) MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153:562–574. PubMedPubMedCentralCrossRefGoogle Scholar
  121. Li S, Liberman LM, Mukherjee N et al (2013b) Integrated detection of natural antisense transcripts using strand-specific RNA sequencing data. Genome Res 23:1730–1739. PubMedPubMedCentralCrossRefGoogle Scholar
  122. Li J, Reichel M, Millar AA (2014) Determinants beyond both complementarity and cleavage govern microR159 efficacy in Arabidopsis. PLoS Genet 10:e1004232. PubMedPubMedCentralCrossRefGoogle Scholar
  123. Li H, Dong Y, Chang J, He J, Chen H, Liu Q, Wei C, Ma J, Zhang Y, Yang J, Zhang X (2016) Throughput MicroRNA and mRNA sequencing reveals that MicroRNAa May be involved in melatoin-mediated cold tolerance in Citrullus lanatus L. Front Plant Sci 7:1231PubMedPubMedCentralGoogle Scholar
  124. Ling J, Luo Z, Liu F, Mao Z, Yang Y, Xie B (2017) Genome-wide analysis of microRNA targeting impacted by SNPs in cucumber genome. Genomics 18:275. PubMedCrossRefGoogle Scholar
  125. Liu J, Carmell M, Rivas FV, Marsden CG, Thomson JM, Song J-J, Hammond SM, Joshua-Tor L, Hannon GJ (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science 305(5689):1437–1441. PubMedCrossRefGoogle Scholar
  126. Liu N, Okamura K, Tyler DM, Phillips MD, Chung W-J, Lai EC (2008) The evolution and functional diversification of animal microRNA genes. Cell Res 18:985–996. PubMedPubMedCentralCrossRefGoogle Scholar
  127. Liu Q, Yao X, Pi L et al (2009) The ARGONAUTE10 gene modulates shoot apical meristem maintenance and establishment of leaf polarity by repressing miR165/166 in Arabidopsis. Plant J 58:27–40. PubMedCrossRefGoogle Scholar
  128. Liu N, Yang J, Guo S, Xu Y, Zhang M (2013a) Genome-wide identification and comparative analysis of conserved and novel microRNAs in grafted watermelon by high-throughput sequencing. PLoS One 8:e57359. PubMedPubMedCentralCrossRefGoogle Scholar
  129. Liu Q, Wang H, Zhu L et al (2013b) Genome-wide identification and analysis of miRNA-related single nucleotide polymorphisms (SNPs) in rice. Rice (N Y) 6:10. CrossRefGoogle Scholar
  130. Liu Y, Wang L, Chen D et al (2014) Genome-wide comparison of microRNAs and their targeted transcripts among leaf, flower and fruit of sweet orange. BMC Genom 15:695. CrossRefGoogle Scholar
  131. Liu W-w, Meng J, Cui J, Luan Y-s (2017) Characterization and Function of MicroRNA*s in Plants. Front Plant Sci 8:2200. PubMedPubMedCentralCrossRefGoogle Scholar
  132. 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 12:2351–2365PubMedPubMedCentralCrossRefGoogle Scholar
  133. Lu Y, Yang X (2010) Computational identification of novel MicroRNAs and their targets in Vigna unguiculata. Comp Funct Genom. CrossRefGoogle Scholar
  134. Lu S, Sun YH, Amerson H, Chiang VL (2007) MicroRNAs in loblolly pine (Pinus taeda L.) and their association with fusiform rust gall development. Plant J 51:1077–1098. PubMedCrossRefGoogle Scholar
  135. Lu S, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in populus. Plant J 55:131–151. PubMedCrossRefGoogle Scholar
  136. Lu S, Sun YH, Chiang VL (2009) Adenylation of plant miRNAs. Nucleic Acids Res 37:1878–1885. PubMedPubMedCentralCrossRefGoogle Scholar
  137. Lv D-K, Bai X, Li Y et al (2010) Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene 459:39–47. PubMedCrossRefGoogle Scholar
  138. Ma X, Tang Z, Qin J, Meng Y (2015) The use of high-throughput sequencing methods for plant microRNA research. RNA Biol 12(7):709–719. PubMedPubMedCentralCrossRefGoogle Scholar
  139. Manavella PA, Hagmann J, Ott F, Laubinger S, Franz M, Macek B, Weigel D (2012) Fast-forward genetics identifies plant CPL phosphatases as regulators of miRNA processing factor HYL1. Cell 151:859–870. PubMedCrossRefGoogle Scholar
  140. Megha S, Basu U, Kav Nat NV (2018) Regulation of low temperature stress in plants by microRNAs. Plant Cell Environ 41:1–15. PubMedCrossRefGoogle Scholar
  141. Meng Y, Gou L, Chen D et al (2010) High-throughput degradome sequencing can be used to gain insights into microRNA precursor metabolism. J Exp Bot 61:3833–3837. PubMedCrossRefGoogle Scholar
  142. Meng Y, Shao C, Wang H, Chen M (2011) The regulatory activities of plant MicroRNAs: a more dynamic perspective. Plant Physiol 157:1583–1595. PubMedPubMedCentralCrossRefGoogle Scholar
  143. Merchan F, Boualem A, Crespi M, Frugier F (2009) Plant polycistronic precursors containing non-homologous microRNAs target transcripts encoding functionally related proteins. Genome Biol 10:R136. PubMedPubMedCentralCrossRefGoogle Scholar
  144. Mickiewicz A, Rybarczyk A, Sarzynska J et al (2016) AmiRNA designer—new method of artificial miRNA design. Acta Biochim Pol 63:71–77. PubMedCrossRefGoogle Scholar
  145. Millar AA, Gubler F (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17:705–721. PubMedPubMedCentralCrossRefGoogle Scholar
  146. Min X, Zhang Z, Liu Y, Wei X, Liu Z, Wang Y, Liu W (2017) Genome-wide development of MicroRNA-Based SSR Markers in Medicago truncatula with their transferability analysis and utilization in related legume species. Int J Mol Sci. CrossRefPubMedPubMedCentralGoogle Scholar
  147. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. PubMedCrossRefGoogle Scholar
  148. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van BF (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309. PubMedCrossRefGoogle Scholar
  149. Mohammed J, Siepel A, Lai EC (2014) Diverse modes of evolutionary emergence and flux of conserved microRNA clusters. RNA 20(12):1850–1863. PubMedPubMedCentralCrossRefGoogle Scholar
  150. Mohorianu I, Stocks MB, Applegate CS et al (2017) The UEA small RNA workbench: a suite of computational tools for small RNA analysis. Methods Mol Biol 1580:193–224. PubMedCrossRefGoogle Scholar
  151. Montes RAC, De Paoli E, Accerbi M, Rymarquis LA, Mahalingam G, Marsch-Martínez N, Mayers BC, Green PJ, de Folter S (2014) Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs. Nature Commun 5:3722. CrossRefGoogle Scholar
  152. Morozova O, Hirst M, Marra MA (2009) Applications of new sequencing technologies for transcriptome analysis. Annu Rev Genom Hum Genet 10:135–151. CrossRefGoogle Scholar
  153. Motameny S, Wolters S, Nürnberg P, Schumacher B (2010) Next generation sequencing of miRNAs—strategies, resources and methods. Genes (Basel) 1:70–84. CrossRefGoogle Scholar
  154. Moxon S, Schwach F, Dalmay T et al (2008) A toolkit for analysing large-scale plant small RNA datasets. Bioinformatics 24:2252–2253. PubMedCrossRefGoogle Scholar
  155. Nagasaki H, Itoh J-i, Hayashi K, Hibara K-i, Satoh-Nagasawa N, Nosaka M, Mukouhata M, Ashikari M, Kitano H, Matsuoka M, Nagato Y, Sato Y (2007) The small interfering RNA production pathway is required for shoot meristem initiation in rice. Proc Natl Acad Sci USA 104:14867–14871. PubMedCrossRefGoogle Scholar
  156. Nair SK, Wang N, Turuspekov Y et al (2010) Cleistogamous flowering in barley arises from the suppression of microRNA-guided HvAP2 mRNA cleavage. Proc Natl Acad Sci 107:490–495. PubMedCrossRefGoogle Scholar
  157. Naqvi AR, Haq QM, Mukherjee SK (2010) MicroRNA profiling of tomato leaf curl new delhi virus (tolcndv) infected tomato leaves indicates that deregulation of mir159/319 and mir172 might be linked with leaf curl disease. Virol J 7:281. PubMedPubMedCentralCrossRefGoogle Scholar
  158. Navarro L, Dunoyer P, Jay F et al (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439. PubMedCrossRefGoogle Scholar
  159. Neilsen CT, Goodall GJ, Bracken CP (2012) IsomiRs–the overlooked repertoire in the dynamic microRNAome. Trends Genet 28:544–549. PubMedCrossRefGoogle Scholar
  160. Niu J, Wang J, Hu H, Chen Y, An J, Cai J, Sun R, Sheng Z, Liu X, Lin S (2016) Cross-talk between freezing response and signaling for regulatory transcriptions of MIR475b and its targets by miR475b promoter in Populus suaveolens. Sci Rep 6:20648. PubMedPubMedCentralCrossRefGoogle Scholar
  161. Nogueira FTS, Madi S, Chitwood DH, Juarez MT, Timmermans MCP (2007) Two small regulatory RNAs establish opposing fates of a developmental axis. Genes Dev 21:750–755. PubMedPubMedCentralCrossRefGoogle Scholar
  162. Nova-Franco B, Íñiguez LP, Valdés-López O et al (2015) The Micro-RNA172c-APETALA2-1 node as a key regulator of the common bean- Rhizobium etli nitrogen fixation symbiosis. Plant Physiol 168:273–291. PubMedPubMedCentralCrossRefGoogle Scholar
  163. Omidvar V, Mohorianu I, Dalmay T, Fellner M (2015) Identification of miRNAs with potential roles in regulation of anther development and male-sterility in 7B-1 male-sterile tomato mutant. BMC Genom 16:878. CrossRefGoogle Scholar
  164. Ossowski S, Schwab R, Weigel D (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J 53:674–690. PubMedCrossRefGoogle Scholar
  165. Ouyang S, Park G, Atamian HS et al (2014) MicroRNAs suppress NB domain genes in tomato that confer resistance to Fusarium oxysporum. PLoS Pathog 10:e1004464. PubMedPubMedCentralCrossRefGoogle Scholar
  166. Pantaleo V, Szittya G, Moxon S et al (2010) Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. Plant J 62:960–976. PubMedCrossRefGoogle Scholar
  167. Park MY, Wu G, Gonzalez-Sulser A, Vaucheret H, Poethig RS (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci USA 102:3691–3696. PubMedCrossRefGoogle Scholar
  168. Patanun O, Lertpanyasampatha M, Sojikul P, Viboonjun U, Narangajavana J (2013) Computational identification of MicroRNAs and their targets in Cassava (Manihot esculenta Crantz.). Mol Biotechnol 53(3):257–269. PubMedCrossRefGoogle Scholar
  169. Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295. PubMedCrossRefGoogle Scholar
  170. Peng T, Sun H, Du Y et al (2013) Characterization and expression patterns of microRNAs involved in rice grain filling. PLoS One 8:e54148. PubMedPubMedCentralCrossRefGoogle Scholar
  171. Piriyapongsa J, Jordan IK (2008) Dual coding of siRNAs and miRNAs by plant transposable elements. RNA 14(5):814–821. PubMedPubMedCentralCrossRefGoogle Scholar
  172. Rajewsky N (2006) microRNA target predictions in animals. Nat Genet 38:8–13. CrossRefGoogle Scholar
  173. Reichel M, Li Y, Li J, Millar AA (2015) Inhibiting plant microRNA activity: molecular SPONGEs, target MIMICs and STTMs all display variable efficacies against target microRNAs. Plant Biotechnol J 13:915–926. PubMedCrossRefGoogle Scholar
  174. Reinhart BJ, Weinstein EG, Rhoades MW et al (2002) MicroRNAs in plants. Genes Dev 16:1616–1626. PubMedPubMedCentralCrossRefGoogle Scholar
  175. Reis RS, Hart-Smith G, Eamens AL et al (2015a) Gene regulation by translational inhibition is determined by Dicer partnering proteins. Nat Plants 1:14027. PubMedCrossRefGoogle Scholar
  176. Reis RS, Hart-Smith G, Eamens AL et al (2015b) MicroRNA regulatory mechanisms play different roles in Arabidopsis. J Proteome Res 14:4743–4751. PubMedCrossRefGoogle Scholar
  177. Reis RS, Eamens AL, Roberts TH, Waterhouse PM (2016) Chimeric DCL1-partnering proteins provide insights into the MicroRNA pathway. Front Plant Sci 6:1201. PubMedPubMedCentralCrossRefGoogle Scholar
  178. Ren G, Xie M, Dou Y, Zhang S, Zhang C, Yu B (2012) Regulation of miRNA abundance by RNA binding protein TOUGH in Arabidopsis. Proc Natl Acad Sci USA 109:12817–12821. PubMedCrossRefGoogle Scholar
  179. Ren G, Xiea M, Zhanga S, Vinovskisa C, Chen X, Yua B (2014) Methylation protects microRNAs from an AGO1—associated activity that uridylates 5′ RNA fragments generated by AGO1 cleavage. Proc Natl Acad Sci USA 111(17):6365–6370. PubMedCrossRefGoogle Scholar
  180. Reynoso MA, Blanco FA, Bailey-Serres J et al (2013) Selective recruitment of mRNAs and miRNAs to polyribosomes in response to rhizobia infection in Medicago truncatula. Plant J 73:289–301. PubMedCrossRefGoogle Scholar
  181. Rhoades MW, Reinhart BJ, Lim LP et al (2002) Prediction of plant microRNA targets. Cell 110:513–520. PubMedCrossRefGoogle Scholar
  182. Rodriguez A, Griffiths-Jones S, Ashurst JL, Bradley A (2004) Identification of mammalian microRNA host genes and transcription units. Genome Res 14(10A):1902–1910. PubMedPubMedCentralCrossRefGoogle Scholar
  183. Rogers K, Chen X (2013) Biogenesis, Turnover, and mode of action of plant MicroRNAs. Plant Cell 25(7):2383–2399. PubMedPubMedCentralCrossRefGoogle Scholar
  184. Ru P, Xu L, Ma H, Huang H (2006) Plant fertility defects induced by the enhanced expression of microRNA167. Cell Res 16:457–465. PubMedCrossRefGoogle Scholar
  185. Ruan M-B, Zhao Y-T, Meng Z-H et al (2009) Conserved miRNA analysis in Gossypium hirsutum through small RNA sequencing. Genomics 94:263–268. PubMedCrossRefGoogle Scholar
  186. Rubio-Somoza I, Weigel D (2011) MicroRNA networks and developmental plasticity in plants. Trends Plant Sci 16:258–264. PubMedCrossRefGoogle Scholar
  187. Rubio-Somoza I, Weigel D (2013) Coordination of flower maturation by a regulatory circuit of three microRNAs. PLoS Genet 9:e1003374. PubMedPubMedCentralCrossRefGoogle Scholar
  188. Rueda A, Barturen G, Lebrón R et al (2015) sRNAtoolbox: an integrated collection of small RNA research tools. Nucleic Acids Res 43:W467–W473. PubMedPubMedCentralCrossRefGoogle Scholar
  189. 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. PubMedCrossRefGoogle Scholar
  190. Sablok G, Srivastva AK, Suprasanna P et al (2015) isomiRs: increasing evidences of isomiRs complexity in plant stress functional biology. Front Plant Sci. CrossRefPubMedPubMedCentralGoogle Scholar
  191. Sakaguchi J, Watanabe Y (2012) miR165⁄166 and the development of land plants. Dev Growth Differ 54:93–99. PubMedCrossRefGoogle Scholar
  192. Sattar S, Addo-Quaye C, Thompson GA (2016) miRNA-mediated auxin signalling repression during Vat -mediated aphid resistance in Cucumis melo. Plant Cell Environ 39:1216–1227. PubMedCrossRefGoogle Scholar
  193. Sawhney VK (1997) Genic male sterility. In: Shivanna KR, Sawhney VK (eds) Pollen Biotechnol. Crop Prod Improv. Cambridge University Press, Cambridge, pp 183–198CrossRefGoogle Scholar
  194. Schwab R, Ossowski S, Riester M et al (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133. PubMedPubMedCentralCrossRefGoogle Scholar
  195. Sha A, Zhao J, Yin K et al (2014) Virus-based MicroRNA silencing in plants. Plant Physiol 164:36–47. PubMedCrossRefGoogle Scholar
  196. Shao H, Wang H, Tang X (2015) NAC transcription factors in plant multiple abiotic stress responses: progress and prospects. Front Plant Sci 6:902. PubMedPubMedCentralCrossRefGoogle Scholar
  197. Shen D, Suhrkamp I, Wang Y et al (2014) Identification and characterization of microRNAs in oilseed rape (Brassica napus) responsive to infection with the pathogenic fungus Verticillium longisporum using Brassica AA (Brassica rapa) and CC (Brassica oleracea) as reference genomes. New Phytol 204:577–594. PubMedCrossRefGoogle Scholar
  198. Shriram V, Kumar V, Devarumath RM, Khare TS, Wani SH (2016) MicroRNAs as potential targets for abiotic stress tolerance in plants. Front Plant Sci 7:817. PubMedPubMedCentralCrossRefGoogle Scholar
  199. Silva GF, Silva EM, da Silva Azevedo M et al (2014) microRNA156-targeted SPL/SBP box transcription factors regulate tomato ovary and fruit development. Plant J 78:604–618. PubMedCrossRefGoogle Scholar
  200. Smoczynska A, Szweykowska-Kulinska Z (2016) MicroRNA-mediated regulation of flower development in grass. Acta Biochim pol 63(4):687–692. PubMedCrossRefGoogle Scholar
  201. Sobkowiak A, Jończyk M, Adamczyk J et al (2016) Molecular foundations of chilling-tolerance of modern maize. BMC Genom 17:125. CrossRefGoogle Scholar
  202. Song JJ, Smith SK, Hannon G, Joshua-Tor L (2004) Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305:1434–1437. PubMedCrossRefGoogle Scholar
  203. Song Q-X, Liu Y-F, Hu X-Y et al (2011) Identification of miRNAs and their target genes in developing soybean seeds by deep sequencing. BMC Plant Biol 11:5. PubMedPubMedCentralCrossRefGoogle Scholar
  204. Song Y, Tian M, Ci D, Zhang D (2015) Methylation of microRNA genes regulates gene expression in bisexual flower development in andromonoecious poplar. J Exp Bot 66:1891–1905. PubMedPubMedCentralCrossRefGoogle Scholar
  205. Song G, Zhang R, Zhang S, Li Y, Gao J, Han X, Chen M, Wang J, Li W, Li G (2017) Response of microRNAs to cold treatment in the young spikes of common wheat. BMC Genom 18:212. CrossRefGoogle Scholar
  206. Souret FF, Kastenmayer JP, Green PJ (2004) AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol Cell 15:173–183. PubMedCrossRefGoogle Scholar
  207. Spanudakis E, Jackson S (2014) The role of microRNAs in the control of flowering time. J Exp Bot 65:365–380. PubMedCrossRefGoogle Scholar
  208. Srivastava PK, Moturu TR, Pandey P et al (2014) A comparison of performance of plant miRNA target prediction tools and the characterization of features for genome-wide target prediction. BMC Genom 15:348. CrossRefGoogle Scholar
  209. Sun C, Zhao Q, Liu D et al (2013) Ectopic expression of the apple Md-miRNA156h gene regulates flower and fruit development in Arabidopsis. Plant Cell Tissue Organ Cult 112:343–351. CrossRefGoogle Scholar
  210. Sun F, Guo G, Du J, Guo W, Peng H, Ni Z, Sun Q, Yao Y (2014) Whole-genome discovery of miRNAs and their targets in wheat (Triticum aestivum). BMC Plant Biol 14:142. PubMedPubMedCentralCrossRefGoogle Scholar
  211. Sunkar R, Zhu J-K (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019. PubMedPubMedCentralCrossRefGoogle Scholar
  212. Sunkar R, Kapoor A, Zhu J-K (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. PubMedPubMedCentralCrossRefGoogle Scholar
  213. Tang Y, Wang F, Zhao J, Xie K, Hong Y, Liu Y (2010) Virus-based MicroRNA expression for gene functional analysis in plants. Plant Physiol 153:632–641. PubMedPubMedCentralCrossRefGoogle Scholar
  214. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  215. Teotia S, Tang G (2015) To bloom or not to bloom: role of microRNAs in plant flowering. Mol Plant 8:359–377. PubMedCrossRefGoogle Scholar
  216. Thatcher SR, Burd S, Wright C et al (2015) Differential expression of miRNAs and their target genes in senescing leaves and siliques: insights from deep sequencing of small RNAs and cleaved target RNAs. Plant Cell Environ 38:188–200. PubMedCrossRefGoogle Scholar
  217. Tiwari M, Sharma D, Trivedi PK (2014) Artificial microRNA mediated gene silencing in plants: progress and perspectives. Plant Mol Biol 86:1–18. PubMedCrossRefGoogle Scholar
  218. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  219. Trumbo JL, Zhang B, Stewart CN (2015) Manipulating microRNAs for improved biomass and biofuels from plant feedstocks. Plant Biotechnol J 13:337–354. PubMedCrossRefGoogle Scholar
  220. Tsuji H, Aya K, Ueguchi-Tanaka M et al (2006) GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J 47:427–444. PubMedCrossRefGoogle Scholar
  221. Turner M, Yu O, Subramanian S (2012) Genome organization and characteristics of soybean microRNAs. BMC Genom 13:169. CrossRefGoogle Scholar
  222. Tyczewska A, Bąkowska-Żywicka K, Gracz J, Twardowski T (2016) Stress responsive non-protein coding RNAs. Agricultural and biological sciences. In: Shanker AK, Shanker C (eds) Abiotic and biotic stress in plants—recent advances and future perspectives, chap 7. InTech, pp 153–181.
  223. Vaistij FE, Elias L, George GL, Jones L (2010) Suppression of microRNA accumulation via RNA interference in Arabidopsis thaliana. Plant Mol Biol 73:391–397. PubMedCrossRefGoogle Scholar
  224. Vallarino JG, Osorio S, Bombarely A et al (2015) Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening. New Phytol 208:482–496. PubMedCrossRefGoogle Scholar
  225. Van Heerden PDR, Kiddle G, Pellny TK, Mokwala PW, Jordaan A, Strauss AJ, de Beer M, Schluter U, Kunert KJ, Foyer C (2008) Regulation of respiration and the oxygen diffusion barrier in soybean protect symbiotic nitrogen fixation from chilling-induced inhibition and shoots from premature senescence. Plant Physiol 148:316–327PubMedPubMedCentralCrossRefGoogle Scholar
  226. Vaucheret H (2008) Plant ARGONAUTES. Trends Plant Sci 13(7):350–358. PubMedCrossRefGoogle Scholar
  227. Vaucheret H, Vazquez F, Crété P, Bartel DP (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18:1187–1197. PubMedPubMedCentralCrossRefGoogle Scholar
  228. Vazquez F, Blevins T, Ailhas J et al (2008) Evolution of Arabidopsis MIR genes generates novel microRNA classes. Nucleic Acids Res 36:6429–6438. PubMedPubMedCentralCrossRefGoogle Scholar
  229. Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687. PubMedCrossRefPubMedCentralGoogle Scholar
  230. Walsh K, Layzell D (1986) Carbon and nitrogen assililation and partitioning in soybeans exposed to low root temperatures. Plant Physiol 80:249–255PubMedPubMedCentralCrossRefGoogle Scholar
  231. Wang JW (2014) Regulation of flowering time by the miR156-mediated age pathway. J Exp Bot 65:4723–4730. PubMedCrossRefGoogle Scholar
  232. Wang JW, Czech B, Weigel D (2009) MIR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749. PubMedCrossRefGoogle Scholar
  233. Wang C, Han J, Liu C et al (2012) Identification of microRNAs from Amur grape (Vitis amurensis Rupr.) by deep sequencing and analysis of microRNA variations with bioinformatics. BMC Genom 13:122. CrossRefGoogle Scholar
  234. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  235. Warthmann N, Chen H, Ossowski S, Weigel D, Herve´ P (2008) Highly specific gene silencing by artificial miRNAs in rice. PLoS One 3(3):e1829. PubMedPubMedCentralCrossRefGoogle Scholar
  236. Wei X, Zhang X, Yao Q et al (2015) The miRNAs and their regulatory networks responsible for pollen abortion in Ogura-CMS Chinese cabbage revealed by high-throughput sequencing of miRNAs, degradomes, and transcriptomes. Front Plant Sci 6:894. PubMedPubMedCentralCrossRefGoogle Scholar
  237. Wong CE, Zhao Y-T, Wang X-J et al (2011) MicroRNAs in the shoot apical meristem of soybean. J Exp Bot 62:2495–2506. PubMedCrossRefGoogle Scholar
  238. Wu L, Fan J, Belasco JG (2006a) MicroRNAs direct rapid deadenylation of mRNA. Proc Natl Acad Sci USA 103(11):4034–4039. PubMedCrossRefGoogle Scholar
  239. Wu M-F, Tian Q, Reed JW (2006b) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133:4211–4218. PubMedCrossRefPubMedCentralGoogle Scholar
  240. Wu L, Zhou H, Zhang Q et al (2010) DNA methylation mediated by a MicroRNA pathway. Mol Cell 38:465–475. PubMedCrossRefGoogle Scholar
  241. Wu J, Liu Q, Wang X et al (2013) mirTools 2.0 for non-coding RNA discovery, profiling, and functional annotation based on high-throughput sequencing. RNA Biol 10:1087–1092. PubMedPubMedCentralCrossRefGoogle Scholar
  242. Wu J, Wang D, Liu Y et al (2014) Identification of miRNAs involved in pear fruit development and quality. BMC Genom 15:953. CrossRefGoogle Scholar
  243. Wu P, Wu Y, Liu C-C et al (2016) Identification of arbuscular mycorrhiza (AM)-responsive microRNAs in tomato. Front Plant Sci 7:429. PubMedPubMedCentralCrossRefGoogle Scholar
  244. Xie Z, Allen E, Fahlgren N, Calamar A, Givan SA, Carrington JC (2005) Expression of Arabidopsis MIRNA genes. Plant Physiol 138:2145–2154. PubMedPubMedCentralCrossRefGoogle Scholar
  245. Xie F, Frazier TP, Zhang B (2010) Identification and characterization of microRNAs and their targets in the bioenergy plant switchgrass (Panicum virgatum). Planta 232:417–434. PubMedCrossRefGoogle Scholar
  246. Xu MY, Zhang L, Li WW et al (2014) Stress-induced early flowering is mediated by miR169 in Arabidopsis thaliana. J Exp Bot 65:89–101. PubMedCrossRefGoogle Scholar
  247. Xuan P, Guo M, Huang Y et al (2011) MaturePred: efficient identification of microRNAs within novel plant pre-miRNAs. PLoS One 6:e27422. PubMedPubMedCentralCrossRefGoogle Scholar
  248. Yan J, Gu Y, Jia X et al (2012) Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis. Plant Cell 24:415–427. PubMedPubMedCentralCrossRefGoogle Scholar
  249. Yan F, Guo W, Wu G et al (2014) A virus-based miRNA suppression (VbMS) system for miRNA loss-of-function analysis in plants. Biotechnol J 9:702–708. PubMedCrossRefGoogle Scholar
  250. Yang X, Li L (2011) miRDeep-P: a computational tool for analyzing the microRNA transcriptome in plants. Bioinformatics 27:2614–2615. PubMedCrossRefGoogle Scholar
  251. Yang L, Wu G, Poethig RS (2012) Mutations in the GW-repeat protein SUO reveal a developmental function for microRNA-mediated translational repression in Arabidopsis. Proc Natl Acad Sci 109:315–320. PubMedCrossRefGoogle Scholar
  252. Yao Y, Guo G, Ni Z, Sunkar R, Du J, Zhu JK, Sun Q (2007) Cloning and characterization of micrfoRNAs from wheat (Triticum aestivum L.). Genome Biol 8:R96. PubMedPubMedCentralCrossRefGoogle Scholar
  253. Yao F, Zhu H, Yi C et al (2015) MicroRNAs and targets in senescent litchi fruit during ambient storage and post-cold storage shelf life. BMC Plant Biol 15:181. PubMedPubMedCentralCrossRefGoogle Scholar
  254. Yin K, Tang Y, Zhao J (2015) Genome-wide characterization of miRNAs involved in N gene-mediated immunity in response to tobacco mosaic virus in Nicotiana benthamiana. Evol Bioinform 11(Suppl 1):1–11. CrossRefGoogle Scholar
  255. Yu B, Yang Z, Li J, Minakhina S, Yang M, Padgett RW, Steward R, Chen X (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307(5711):932–935. PubMedPubMedCentralCrossRefGoogle Scholar
  256. Yu B, Bi L, Zheng B, Ji L, Chevalier D, Agarwal M et al (2008) The FHA proteins DAWDLE in Arabidopsis and SNIP1 in humans act in small RNA biogenesis. Proc Natl Acad Sci USA 105:10073–10078. PubMedCrossRefGoogle Scholar
  257. Zeng C, Wang W, Zheng Y et al (2010) Conservation and divergence of microRNAs and their functions in Euphorbiaceous plants. Nucleic Acids Res 38:981–995. PubMedCrossRefGoogle Scholar
  258. Zeng H, Wang G, Hu X, Wang H, Du L, Zhu Y (2014) Role of microRNAs in plant responses to nutrient stress. Plant Soil 374:1005–1021. CrossRefGoogle Scholar
  259. Zhang B (2015) MicroRNA: a new target for improving plant tolerance to abiotic stress. J Exp Bot 66:1749–1761. PubMedPubMedCentralCrossRefGoogle Scholar
  260. Zhang BH, Pan XP, Cox SB, Cobb GP, Anderson TA (2006) Evidence that miRNAs are different from other RNAs. Cell Mol Life Sci 63(2):246–254. PubMedCrossRefGoogle Scholar
  261. Zhang J, Xu Y, Huan Q, Chong K (2009) Deep sequencing of Brachypodium small RNAs at the global genome level identifies microRNAs involved in cold stress response. BMC Genom 10:449. CrossRefGoogle Scholar
  262. Zhang W, Gao S, Zhou X et al (2011) Bacteria-responsive microRNAs regulate plant innate immunity by modulating plant hormone networks. Plant Mol Biol 75:93–105. PubMedCrossRefGoogle Scholar
  263. Zhang S, Yue Y, Sheng L et al (2013) PASmiR: a literature-curated database for miRNA molecular regulation in plant response to abiotic stress. BMC Plant Biol 13:33. PubMedPubMedCentralCrossRefGoogle Scholar
  264. Zhang S, Wang Y, Li K et al (2014) Identification of cold-responsive miRNAs and their target genes in nitrogen-fixing nodules of soybean. Int J Mol Sci 15:13596–13614. PubMedPubMedCentralCrossRefGoogle Scholar
  265. Zhang Y, Wang W, Chen J, Liu J, Xia M, Shen F (2015) Identification of miRNAs and their targets in cotton inoculated with Verticillium dahliae by high-throughput sequencing and degradome analysis. Int J Mol Sci 16:14749–14768. PubMedPubMedCentralCrossRefGoogle Scholar
  266. Zhang Y, Zang Q, Xu B et al (2016) IsomiR Bank: a research resource for tracking IsomiRs. Bioinformatics 32:2069–2071. PubMedCrossRefGoogle Scholar
  267. Zhang H, Zhang J, Yan J, Gou F, Mao Y, Tang G, Botella JR, Zhua J-K (2017) Short tandem target mimic rice lines uncover functions of miRNAs in regulating important agronomic traits. Proc Natl Acad Sci USA 114:5277–5282. PubMedCrossRefGoogle Scholar
  268. Zhao X, Li L (2013) Comparative analysis of microRNA promoters in Arabidopsis and rice. Genom Proteom Bioinform 11:56–60. CrossRefGoogle Scholar
  269. Zhao R, Dielen V, Kinet JM, Boutry M (2000) Cosuppression of a plasma membrane H(+)-ATPase isoform impairs sucrose translocation, stomatal opening, plant growth, and male fertility. Plant Cell 12:535–546PubMedPubMedCentralGoogle Scholar
  270. Zhao W, Li Z, Fan J et al (2015) Identification of jasmonic acid-associated microRNAs and characterization of the regulatory roles of the miR319/TCP4 module under root-knot nematode stress in tomato. J Exp Bot 66:4653–4667. PubMedPubMedCentralCrossRefGoogle Scholar
  271. Zhao Y, Wang F, Chen S, Wan J, Wang G (2017) Methods of MicroRNA promoter prediction and transcription factor mediated regulatory network. BioMed Res Int 2017:8. CrossRefGoogle Scholar
  272. Zheng L-L, Qu L-H (2015) Application of microRNA gene resources in the improvement of agronomic traits in rice. Plant Biotechnol J 13:329–336. PubMedCrossRefGoogle Scholar
  273. Zhou M, Luo H (2013) MicroRNA-mediated gene regulation: potential applications for plant genetic engineering. Plant Mol Biol 83:59–75. PubMedCrossRefGoogle Scholar
  274. Zhou X, Wang G, Sutoh K et al (2008) Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochim Biophys Acta 1779:780–788. PubMedCrossRefGoogle Scholar
  275. Zhou Y, Honda M, Zhu H et al (2015) Spatiotemporal sequestration of miR165/166 by Arabidopsis argonaute10 promotes shoot apical meristem maintenance. Cell Rep 10:1819–1827. PubMedCrossRefGoogle Scholar
  276. Zhu D, Deng XW (2012) A non-coding RNA locus mediates environment-conditioned male sterility in rice. Cell Res 22(5):791–792. PubMedPubMedCentralCrossRefGoogle Scholar
  277. Zielezinski A, Dolata J, Alaba S, Kruszka K, Pacak A, Swida-Barteczka A et al (2015) mirEX 2.0—an integrated environment for expression profiling of plant microRNAs. BMC Plant Biotechnol 15:144. CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2018

Authors and Affiliations

  • Maria Szwacka
    • 1
    Email author
  • Magdalena Pawełkowicz
    • 1
  • Agnieszka Skarzyńska
    • 1
  • Paweł Osipowski
    • 1
  • Michał Wojcieszek
    • 1
  • Zbigniew Przybecki
    • 1
  • Wojciech Pląder
    • 1
    Email author
  1. 1.Department of Plant Genetics, Breeding and Biotechnology, Faculty of Horticulture, Biotechnology and Landscape ArchitectureWarsaw University of Life Sciences, SGGWWarsawPoland

Personalised recommendations