Plant Molecular Biology

, Volume 86, Issue 1–2, pp 1–18 | Cite as

Artificial microRNA mediated gene silencing in plants: progress and perspectives

  • Manish Tiwari
  • Deepika Sharma
  • Prabodh Kumar Trivedi
Review

Abstract

Homology based gene silencing has emerged as a convenient approach for repressing expression of genes in order to study their functions. For this purpose, several antisense or small interfering RNA based gene silencing techniques have been frequently employed in plant research. Artificial microRNAs (amiRNAs) mediated gene silencing represents one of such techniques which can utilize as a potential tool in functional genomics. Similar to microRNAs, amiRNAs are single-stranded, approximately 21 nt long, and designed by replacing the mature miRNA sequences of duplex within pre-miRNAs. These amiRNAs are processed via small RNA biogenesis and silencing machinery and deregulate target expression. Holding to various refinements, amiRNA technology offers several advantages over other gene silencing methods. This is a powerful and robust tool, and could be applied to unravel new insight of metabolic pathways and gene functions across the various disciplines as well as in translating observations for improving favourable traits in plants. This review highlights general background of small RNAs, improvements made in RNAi based gene silencing, implications of amiRNA in gene silencing, and describes future themes for improving value of this technology in plant science.

Keywords

amiRNA miRNA RNA silencing Gene expression Plant biotechnology Stress response 

References

  1. Ai T, Zhang L, Gao Z, Zhu CX, Guo X (2011) Highly efficient virus resistance mediated by artificial microRNAs that target the suppressor of PVX and PVY in plants. Plant Biol (Stuttg) 13:304–316CrossRefGoogle Scholar
  2. Alvarez JP, Pekker I, Goldshmidt A, Blum E, Amsellem Z, Eshed Y (2006) Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18:1134–1151PubMedCentralPubMedCrossRefGoogle Scholar
  3. Axtell MJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64:137–159PubMedCrossRefGoogle Scholar
  4. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297PubMedCrossRefGoogle Scholar
  5. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233PubMedCentralPubMedCrossRefGoogle Scholar
  6. Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363PubMedCrossRefGoogle Scholar
  7. Belide S, Petrie JR, Shrestha P, Singh SP (2012) Modification of seed oil composition in Arabidopsis by artificial microRNA-mediated gene silencing. Front Plant Sci 3:168PubMedCentralPubMedCrossRefGoogle Scholar
  8. Bollman KM, Aukerman MJ, Park MY, Hunter C, Berardini TZ, Poethig RS (2003) HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis. Development 130:1493–1504PubMedCrossRefGoogle Scholar
  9. Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigel D (2007) Autoimmune response as a mechanism for a Dobzhansky–Muller-type incompatibility syndrome in plants. PLoS Biol 5:e236PubMedCentralPubMedCrossRefGoogle Scholar
  10. Brodersen P, Voinnet O (2006) The diversity of RNA silencing pathways in plants. Trends Genet 22:268–280PubMedCrossRefGoogle Scholar
  11. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190PubMedCrossRefGoogle Scholar
  12. Burgess SJ, Tredwell G, Molnàr A, Bundy JG, Nixon PJ (2012) Artificial microRNA-mediated knockdown of pyruvate formate lyase (PFL1) provides evidence for an active 3-hydroxybutyrate production pathway in the green alga Chlamydomonas reinhardtii. J Biotechnol 162:57–66Google Scholar
  13. Butardo VM, Fitzgerald MA, Bird AR, Gidley MJ, Flanagan BM, Larroque O, Resurreccion AP, Laidlaw HK, Jobling SA, Morell MK, Rahman S (2011) Impact of down-regulation of starch branching enzyme IIb in rice by artificial microRNA- and hairpin RNA-mediated RNA silencing. J Exp Bot 62:4927–4941PubMedCentralPubMedCrossRefGoogle Scholar
  14. Carbonell A, Takeda A, Fahlgren N, Johnson SC, Cuperus JT, Carrington JC (2014) New generation of artificial microRNA and synthetic trans-acting small interfering RNA vectors for efficient gene silencing in Arabidopsis. Plant Physiol 165:15–29PubMedCentralPubMedCrossRefGoogle Scholar
  15. Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–655PubMedCentralPubMedCrossRefGoogle Scholar
  16. Chen X (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25:21–44PubMedCrossRefGoogle Scholar
  17. Chen S, Yang Y, Shi W, Ji Q, He F, Zhang Z, Cheng Z, Liu X, Xu M (2008) Badh2, encoding betaine aldehyde dehydrogenase, inhibits the biosynthesis of 2-acetyl-1-pyrroline, a major component in rice fragrance. Plant Cell 20:1850–1861PubMedCentralPubMedCrossRefGoogle Scholar
  18. Chen M, Wei X, Shao G, Tang S, Luo J, Hu P (2012) Fragrance of rice grain achieved via artificial micro-RNA induced down-regulation of OsBADH2. Plant Breed 131:584–590CrossRefGoogle Scholar
  19. Chen H, Jiang S, Zheng J, Lin Y (2013a) Improving panicle exsertion of rice cytoplasmic male sterile line by combination of artificial microRNA and artificial target mimic. Plant Biotechnol J 11:336–343PubMedCrossRefGoogle Scholar
  20. Chen Y, Chen Z, Kang J, Kang D, Gu H, Qin G (2013b) AtMYB14 regulates cold tolerance in Arabidopsis. Plant Mol Biol Rep 31:87–97PubMedCentralPubMedCrossRefGoogle Scholar
  21. Coimbra S, Costa M, Jones B, Mendes MA, Pereira LG (2009) Pollen grain development is compromised in Arabidopsis agp6 agp11 null mutants. J Exp Bot 60:3133–3142PubMedCentralPubMedCrossRefGoogle Scholar
  22. Cuperus JT, Fahlgren N, Carrington JC (2011) Evolution and functional diversification of miRNA genes. Plant Cell 23:431–442PubMedCentralPubMedCrossRefGoogle Scholar
  23. Dalmay T, Hamilton A, Mueller E, Baulcombe DC (2000) Potato virus X amplicons in Arabidopsis mediate genetic and epigenetic gene silencing. Plant Cell 12:369–379PubMedCentralPubMedCrossRefGoogle Scholar
  24. de Lima JC, Loss-Morais G, Margis R (2012) MicroRNAs play critical roles during plant development and in response to abiotic stresses. Genet Mol Biol 35:1069–1077PubMedCentralPubMedCrossRefGoogle Scholar
  25. Ding XS, Schneider WL, Chaluvadi SR, Mian MA, Nelson RS (2006) Characterization of a Brome mosaic virus strain and its use as a vector for gene silencing in monocotyledonous hosts. Mol Plant Microbe Interact 19:1229–1239PubMedCrossRefGoogle Scholar
  26. Ding Y, Chen Z, Zhu C (2011) Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J Exp Bot 62:3563–3573PubMedCentralPubMedCrossRefGoogle Scholar
  27. Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AA (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633PubMedCrossRefGoogle Scholar
  28. Duan CG, Wang CH, Fang RX, Guo HS (2008) Artificial microRNAs highly accessible to targets confer efficient virus resistance in plants. J Virol 82:11084–11095PubMedCentralPubMedCrossRefGoogle Scholar
  29. Eamens AL, Wang MB (2011) Alternate approaches to repress endogenous microRNA activity in Arabidopsis thaliana. Plant Signal Behav 6:349–359PubMedCentralPubMedCrossRefGoogle Scholar
  30. Eamens AL, Agius C, Smith NA, Waterhouse PM, Wang MB (2011) Efficient silencing of endogenous microRNAs using artificial microRNAs in Arabidopsis thaliana. Mol Plant 4:157–170Google Scholar
  31. Fahim M, Millar AA, Wood CC, Larkin PJ (2012) Resistance to Wheat streak mosaic virus generated by expression of an artificial polycistronic microRNA in wheat. Plant Biotechnol J 10:150–163PubMedCrossRefGoogle Scholar
  32. Fahlgren N, Jogdeo S, Kasschau KD, Sullivan CM, Chapman EJ, Laubinger S, Smith LM, Dasenko M, Givan SA, Weigel D, Carrington JC (2010) MicroRNA gene evolution in Arabidopsis lyrata and Arabidopsis thaliana. Plant Cell 22:1074–1089PubMedCentralPubMedCrossRefGoogle Scholar
  33. Felippes FF, Wang JW, Weigel D (2012) MIGS: miRNA-induced gene silencing. Plant J 70:541–547PubMedCrossRefGoogle Scholar
  34. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811PubMedCrossRefGoogle Scholar
  35. Ghildiyal M, Zamore PD (2009) Small silencing RNAs: an expanding universe. Nat Rev Genet 10:94–108PubMedCentralPubMedCrossRefGoogle Scholar
  36. Haney CH, Long SR (2010) Plant flotillins are required for infection by nitrogen-fixing bacteria. Proc Natl Acad Sci USA 107:478–483PubMedCentralPubMedCrossRefGoogle Scholar
  37. Harmoko R, Fanata WI, Yoo JY, Ko KS, Rim YG, Uddin MN, Siswoyo TA, Lee SS, Kim DY, Lee SY, Lee KO (2013) RNA-dependent RNA polymerase 6 is required for efficient hpRNA-induced gene silencing in plants. Mol Cells 35:202–209PubMedCentralPubMedCrossRefGoogle Scholar
  38. Hauser F, Chen W, Deinlein U, Chang K, Ossowski S, Fitz J, Hannon GJ, Schroeder JI (2013) A genomic-scale artificial microRNA library as a tool to investigate the functionally redundant gene space in Arabidopsis. Plant Cell 25:2848–2863PubMedCentralPubMedCrossRefGoogle Scholar
  39. He H, He L, Gu M (2014) Role of microRNAs in aluminum stress in plants. Plant Cell Rep 33:831–836PubMedCrossRefGoogle Scholar
  40. Hein I, Barciszewska-Pacak M, Hrubikova K, Williamson S, Dinesen M, Soenderby IE, Sundar S, Jarmolowski A, Shirasu K, Lacomme C (2005) Virus-induced gene silencing-based functional characterization of genes associated with powdery mildew resistance in barley. Plant Physiol 138:2155–2164PubMedCentralPubMedCrossRefGoogle Scholar
  41. Henderson IR, Zhang X, Lu C, Johnson L, Meyers BC, Green PJ, Jacobsen SE (2006) Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nat Genet 38:721–725PubMedCrossRefGoogle Scholar
  42. Hidalgo O, Bartholmes C, Gleissberg S (2012) Virus-induced gene silencing (VIGS) in Cysticapnos vesicaria, a zygomorphic-flowered Papaveraceae (Ranunculales, basal eudicots). Ann Bot 109:911–920PubMedCentralPubMedCrossRefGoogle Scholar
  43. Hileman LC, Drea S, Martino G, Litt A, Irish VF (2005) Virus-induced gene silencing is an effective tool for assaying gene function in the basal eudicot species Papaver somniferum (opium poppy). Plant J 44:334–341PubMedCrossRefGoogle Scholar
  44. Iwakawa HO, Tomari Y (2013) Molecular insights into microRNA-mediated translational repression in plants. Mol Cell 52:591–601PubMedCrossRefGoogle Scholar
  45. Jelly NS, Schellenbaum P, Walter B, Maillot P (2012) Transient expression of artificial microRNAs targeting Grapevine fanleaf virus and evidence for RNA silencing in grapevine somatic embryos. Transgenic Res 21:1319–1327PubMedCrossRefGoogle Scholar
  46. Jover-Gil S, Candela H, Ponce MR (2005) Plant microRNAs and development. Int J Dev Biol 49:733–744PubMedGoogle Scholar
  47. Khraiwesh B, Ossowski S, Weigel D, Reski R, Frank W (2008) Specific gene silencing by artificial microRNAs in Physcomitrella patens: an alternative to targeted gene knockouts. Plant Physiol 148:684–693PubMedCentralPubMedCrossRefGoogle Scholar
  48. Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819:137–148PubMedCentralPubMedCrossRefGoogle Scholar
  49. Kim J, Somers DE (2010) Rapid assessment of gene function in the circadian clock using artificial microRNA in Arabidopsis mesophyll protoplasts. Plant Physiol 154:611–621PubMedCentralPubMedCrossRefGoogle Scholar
  50. Kruszka K, Pieczynski M, Windels D, Bielewicz D, Jarmolowski A, Szweykowska-Kulinska Z, Vazquez F (2012) Role of microRNAs and other sRNAs of plants in their changing environments. J Plant Physiol 169:1664–1672PubMedCrossRefGoogle Scholar
  51. Kung YJ, Lin SS, Huang YL, Chen TC, Harish SS, Chua NH, Yeh SD (2012) Multiple artificial microRNAs targeting conserved motifs of the replicase gene confer robust transgenic resistance to negative-sense single-stranded RNA plant virus. Mol Plant Pathol 13:303–317PubMedCrossRefGoogle Scholar
  52. Latijnhouwers M, Xu XM, Moller SG (2010) Arabidopsis stromal 70-kDa heat shock proteins are essential for chloroplast development. Planta 232:567–578PubMedCrossRefGoogle Scholar
  53. Lau NC, Lim LP, Weinstein EG, Bartel DP (2001) An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294:858–862PubMedCrossRefGoogle Scholar
  54. Lee RC, Ambros V (2001) An extensive class of small RNAs in Caenorhabditis elegans. Science 294:862–864PubMedCrossRefGoogle Scholar
  55. Li C, Wei J, Lin Y, Chen H (2012) Gene silencing using the recessive rice bacterial blight resistance gene xa13 as a new paradigm in plant breeding. Plant Cell Rep 31:851–862PubMedCrossRefGoogle Scholar
  56. Li S, Liu L, Zhuang X, Yu Y, Liu X, Cui X, Ji L, Pan Z, Cao X, Mo B, Zhang F, Raikhel N, Jiang L, Chen X (2013) MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153:562–574PubMedCentralPubMedCrossRefGoogle Scholar
  57. Li JF, Zhang D, Sheen J (2014) Epitope-tagged protein-based artificial miRNA screens for optimized gene silencing in plants. Nat Protoc 9:939–949PubMedCrossRefGoogle Scholar
  58. Liang G, He H, Li Y, Yu D (2012) A new strategy for construction of artificial miRNA vectors in Arabidopsis. Planta 235:1421–1429PubMedCrossRefGoogle Scholar
  59. Lim LP, Glasner ME, Yekta S, Burge CB, Bartel DP (2003) Vertebrate microRNA genes. Science 299:1540PubMedCrossRefGoogle Scholar
  60. Ling H, Fabbri M, Calin GA (2013) MicroRNAs and other non-coding RNAs as targets for anticancer drug development. Nat Rev Drug Discov 12:847–865PubMedCrossRefGoogle Scholar
  61. Liscombe DK, O’Connor SE (2011) A virus-induced gene silencing approach to understanding alkaloid metabolism in Catharanthus roseus. Phytochemistry 72:1969–1977PubMedCentralPubMedCrossRefGoogle Scholar
  62. Liu Y, Schiff M, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. Plant J 31:777–786PubMedCrossRefGoogle Scholar
  63. Llave C (2010) Virus-derived small interfering RNAs at the core of plant-virus interactions. Trends Plant Sci 15:701–707PubMedCrossRefGoogle Scholar
  64. Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14:1605–1619PubMedCentralPubMedCrossRefGoogle Scholar
  65. Ma M, Yan Y, Huang L, Chen M, Zhao H (2012) Virus-induced gene-silencing in wheat spikes and grains and its application in functional analysis of HMW-GS-encoding genes. BMC Plant Biol 12:141PubMedCentralPubMedCrossRefGoogle Scholar
  66. Ma X, Cao X, Mo B, Chen X (2013) Trip to ER: MicroRNA-mediated translational repression in plants. RNA Biol 10:1582–1592Google Scholar
  67. McHale M, Eamens AL, Finnegan EJ, Waterhouse PM (2013) A 22-nt artificial microRNA mediates widespread RNA silencing in Arabidopsis. Plant J 76:519–529PubMedCrossRefGoogle Scholar
  68. Melito S, Heuberger AL, Cook D, Diers BW, MacGuidwin AE, Bent AF (2010) A nematode demographics assay in transgenic roots reveals no significant impacts of the Rhg1 locus LRR-Kinase on soybean cyst nematode resistance. BMC Plant Biol 10:104PubMedCentralPubMedCrossRefGoogle Scholar
  69. Meng Y, Chen D, Jin Y, Mao C, Wu P, Chen M (2010) RNA editing of nuclear transcripts in Arabidopsis thaliana. BMC Genom 11:S12CrossRefGoogle Scholar
  70. Meng X, Muszynski MG, Danilevskaya ON (2011) The FT-like ZCN8 gene functions as a floral activator and is involved in photoperiod sensitivity in maize. Plant Cell 23:942–960PubMedCentralPubMedCrossRefGoogle Scholar
  71. Misra P, Pandey A, Tiwari M, Chandrashekar K, Sidhu OP, Asif MH, Chakrabarty D, Singh PK, Trivedi PK, Nath P, Tuli R (2010) Modulation of transcriptome and metabolome of tobacco by Arabidopsis transcription factor, AtMYB12, leads to insect resistance. Plant Physiol 152:2258–2268PubMedCentralPubMedCrossRefGoogle Scholar
  72. Molnar A, Bassett A, Thuenemann E, Schwach F, Karkare S, Ossowski S, Weigel D, Baulcombe D (2009) Highly specific gene silencing by artificial microRNAs in the unicellular alga Chlamydomonas reinhardtii. Plant J 58:165–174Google Scholar
  73. Niu QW, Lin SS, Reyes JL, Chen KC, Wu HW, Yeh SD, Chua NH (2006) Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat Biotechnol 24:1420–1428PubMedCrossRefGoogle Scholar
  74. Ossowski S, Schwab R, Weigel D (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J 53:674–690PubMedCrossRefGoogle Scholar
  75. Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci USA 95:8660–8664PubMedCentralPubMedCrossRefGoogle Scholar
  76. Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263PubMedCrossRefGoogle Scholar
  77. Pandey A, Misra P, Chandrashekar K, Trivedi PK (2012) Development of AtMYB12-expressing transgenic tobacco callus culture for production of rutin with biopesticidal potential. Plant Cell Rep 31:1867–1876PubMedCrossRefGoogle Scholar
  78. Pieczynski M, Marczewski W, Hennig J, Dolata J, Bielewicz D, Piontek P, Wyrzykowska A, Krusiewicz D, Strzelczyk-Zyta D, Konopka-Postupolska D, Krzeslowska M, Jarmolowski A, Szweykowska-Kulinska Z (2013) Down-regulation of CBP80 gene expression as a strategy to engineer a drought-tolerant potato. Plant Biotechnol J 11:459–469PubMedCrossRefGoogle Scholar
  79. Poulsen C, Vaucheret H, Brodersen P (2013) Lessons on RNA silencing mechanisms in plants from eukaryotic argonaute structures. Plant Cell 25:22–37PubMedCentralPubMedCrossRefGoogle Scholar
  80. Pumplin N, Voinnet O (2013) RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat Rev Microbiol 11:745–760PubMedCrossRefGoogle Scholar
  81. Qu J, Ye J, Fang R (2007) Artificial microRNA-mediated virus resistance in plants. J Virol 81:6690–6699PubMedCentralPubMedCrossRefGoogle Scholar
  82. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626PubMedCentralPubMedCrossRefGoogle Scholar
  83. Reyes CA, De Francesco A, Pena EJ, Costa N, Plata MI, Sendin L, Castagnaro AP, Garcia ML (2011) Resistance to Citrus psorosis virus in transgenic sweet orange plants is triggered by coat protein-RNA silencing. J Biotechnol 151:151–158PubMedCrossRefGoogle Scholar
  84. Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60:485–510PubMedCrossRefGoogle Scholar
  85. Sablok G, Perez-Quintero AL, Hassan M, Tatarinova TV, Lopez C (2011) Artificial microRNAs (amiRNAs) engineering—on how microRNA-based silencing methods have affected current plant silencing research. Biochem Biophys Res Commun 406:315–319PubMedCrossRefGoogle Scholar
  86. Schmollinger S, Strenkert D, Schroda M (2010) An inducible artificial microRNA system for Chlamydomonas reinhardtii confirms a key role for heat shock factor 1 in regulating thermotolerance. Curr Genet 56:383–389PubMedCrossRefGoogle Scholar
  87. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133PubMedCentralPubMedCrossRefGoogle Scholar
  88. Schwartz C, Balasubramanian S, Warthmann N, Michael TP, Lempe J, Sureshkumar S, Kobayashi Y, Maloof JN, Borevitz JO, Chory J, Weigel D (2009) Cis-regulatory changes at Flowering Locus T mediate natural variation in flowering responses Arabidopsis thaliana. Genetics 183:723–732PubMedCentralPubMedCrossRefGoogle Scholar
  89. Senthil-Kumar M, Mysore KS (2011) New dimensions for VIGS in plant functional genomics. Trends Plant Sci 16:656–665PubMedCrossRefGoogle Scholar
  90. Shekhawat UK, Ganapathi TR, Hadapad AB (2012) Transgenic banana plants expressing small interfering RNAs targeted against viral replication initiation gene display high-level resistance to banana bunchy top virus infection. J Gen Virol 93:1804–1813PubMedCrossRefGoogle Scholar
  91. Shi R, Yang C, Lu S, Sederoff R, Chiang VL (2010) Specific down-regulation of PAL genes by artificial microRNAs in Populus trichocarpa. Planta 232:1281–1288PubMedCrossRefGoogle Scholar
  92. Simón-Mateo C, García JA (2006) MicroRNA-guided processing impairs Plum pox virus replication, but the virus readily evolves to escape this silencing mechanism. J Virol 80:2429–2436Google Scholar
  93. Smith CJS, Watson CF, Ray J, Bird CR, Morris PC, Schuch W, Grierson D (1988) Antisense RNA inhibition of polygalacturonase gene expression in transgenic tomatoes. Nature 334:724–726CrossRefGoogle Scholar
  94. Sunkar R, Li YF, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203PubMedCrossRefGoogle Scholar
  95. 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 40:291–296PubMedCrossRefGoogle Scholar
  96. Tang Y, Lai Y, Liu Y (2013) Virus-induced gene silencing using artificial miRNAs in Nicotiana benthamiana. Methods Mol Biol 975:99–107PubMedCrossRefGoogle Scholar
  97. Toppino L, Kooiker M, Lindner M, Dreni L, Rotino GL, Kater MM (2011) Reversible male sterility in eggplant (Solanum melongena L.) by artificial microRNA-mediated silencing of general transcription factor genes. Plant Biotechnol J 9:684–692PubMedCrossRefGoogle Scholar
  98. Unver T, Budak H (2009) Virus-induced gene silencing, a post transcriptional gene silencing method. Int J Plant Genomics 2009:198680PubMedCentralPubMedGoogle Scholar
  99. Vaistij FE, Elias L, George GL, Jones L (2010) Suppression of microRNA accumulation via RNA interference in Arabidopsis thaliana. Plant Mol Biol 73:391–397PubMedCrossRefGoogle Scholar
  100. van der Krol AR, Mur LA, Beld M, Mol JN, Stuitje AR (1990) Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 2:291–299PubMedCentralPubMedCrossRefGoogle Scholar
  101. Vaucheret H, Vazquez F, Crete 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 18:1187–1197PubMedCentralPubMedCrossRefGoogle Scholar
  102. Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687PubMedCrossRefGoogle Scholar
  103. Vu TV, Choudhury NR, Mukherjee SK (2013) Transgenic tomato plants expressing artificial microRNAs for silencing the pre-coat and coat proteins of a begomovirus, Tomato leaf curl New Delhi virus, show tolerance to virus infection. Virus Res 172:35–45Google Scholar
  104. Wang X, Yang Y, Zhou J, Yu C, Cheng Y, Yan C, Chen J (2012) Two-step method for constructing Arabidopsis artificial microRNA vectors. Biotechnol Lett 34:1343–1349PubMedCrossRefGoogle Scholar
  105. Warthmann N, Chen H, Ossowski S, Weigel D, Herve P (2008) Highly specific gene silencing by artificial miRNAs in rice. PLoS One 3:e1829PubMedCentralPubMedCrossRefGoogle Scholar
  106. Wassenegger M, Krczal G (2006) Nomenclature and functions of RNA-directed RNA polymerases. Trends Plant Sci 11:142–151PubMedCrossRefGoogle Scholar
  107. Watson JM, Fusaro AF, Wang M, Waterhouse PM (2005) RNA silencing platforms in plants. FEBS Lett 579:5982–5987PubMedCrossRefGoogle Scholar
  108. Wege S, Scholz A, Gleissberg S, Becker A (2007) Highly efficient virus-induced gene silencing (VIGS) in California poppy (Eschscholzia californica): an evaluation of VIGS as a strategy to obtain functional data from non-model plants. Ann Bot 100:641–649PubMedCentralPubMedCrossRefGoogle Scholar
  109. Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y (2010) DNA methylation mediated by a microRNA pathway. Mol Cell 38:465–475PubMedCrossRefGoogle Scholar
  110. Xiao YH, Yin MH, Hou L, Pei Y (2006) Direct amplification of intron-containing hairpin RNA construct from genomic DNA. Biotechniques 41:548–552PubMedCrossRefGoogle Scholar
  111. Xin M, Wang Y, Yao Y, Xie C, Peng H, Ni Z, Sun Q (2010) Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biol 10:123PubMedCentralPubMedCrossRefGoogle Scholar
  112. Xu L, Wang Y, Zhai L, Xu Y, Wang L, Zhu X, Gong Y, Yu R, Limera C, Liu L (2013) Genome-wide identification and characterization of cadmium-responsive microRNAs and their target genes in radish (Raphanus sativus L.) roots. J Exp Bot 64:4271–4287PubMedCentralPubMedCrossRefGoogle Scholar
  113. Yan H, Deng X, Cao Y, Huang J, Ma L, Zhao B (2011a) A novel approach for the construction of plant amiRNA expression vectors. J Biotechnol 151:9–14PubMedCrossRefGoogle Scholar
  114. Yan H, Zhong X, Jiang S, Zhai C, Ma L (2011b) Improved method for constructing plant amiRNA vectors with blue-white screening and MAGIC. Biotechnol Lett 33:1683–1688PubMedCrossRefGoogle Scholar
  115. Yan J, Gu Y, Jia X, Kang W, Pan S, Tang X, Chen X, Tang G (2012a) Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis. Plant Cell 24:415–427PubMedCentralPubMedCrossRefGoogle Scholar
  116. Yan P, Shen W, Gao X, Li X, Zhou P, Duan J (2012b) High-throughput construction of intron-containing hairpin RNA vectors for RNAi in plants. PLoS One 7:e38186PubMedCentralPubMedCrossRefGoogle Scholar
  117. Yeoh CC, Balcerowicz M, Laurie R, Macknight R, Putterill J (2011) Developing a method for customized induction of flowering. BMC Biotechnol 11:36PubMedCentralPubMedCrossRefGoogle Scholar
  118. Yoshikawa M (2013) Biogenesis of trans-acting siRNAs, endogenous secondary siRNAs in plants. Genes Genet Syst 88:77–84PubMedGoogle Scholar
  119. Yoshikawa M, Peragine A, Park MY, Poethig RS (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19:2164–2175PubMedCentralPubMedCrossRefGoogle Scholar
  120. Youseff BH, Rappleye CA (2012) RNAi-based gene silencing using a GFP sentinel system in histoplasma capsulatum. Methods Mol Biol 845:151–164PubMedCrossRefGoogle Scholar
  121. Zhang H, Li L (2013) SQUAMOSA promoter binding protein-like7 regulated microRNA408 is required for vegetative development in Arabidopsis. Plant J 74:98–109PubMedCrossRefGoogle Scholar
  122. Zhang X, Li H, Zhang J, Zhang C, Gong P, Ziaf K, Xiao F, Ye Z (2011) Expression of artificial microRNAs in tomato confers efficient and stable virus resistance in a cell-autonomous manner. Transgenic Res 20:569–581PubMedCrossRefGoogle Scholar
  123. Zhang SG, Liu CY, Li L, Sun TW, Luo YG, Yun WJ, Zhang JY (2013) Examination of artificial MiRNA mimics with centered-site complementarity for gene targeting. PLoS One 8:e72062PubMedCentralPubMedCrossRefGoogle Scholar
  124. Zhou J, Yu F, Chen B, Wang X, Yang Y, Cheng Y, Yan C, Chen J (2013) Universal vectors for constructing artificial microRNAs in plants. Biotechnol Lett 35:1127–1133PubMedCrossRefGoogle Scholar
  125. Zrachya A, Kumar PP, Ramakrishnan U, Levy Y, Loyter A, Arazi T, Lapidot M, Gafni Y (2007) Production of siRNA targeted against TYLCV coat protein transcripts leads to silencing of its expression and resistance to the virus. Transgenic Res 16:385–398PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Manish Tiwari
    • 1
  • Deepika Sharma
    • 1
    • 2
  • Prabodh Kumar Trivedi
    • 1
    • 2
  1. 1.Council of Scientific and Industrial Research-National Botanical Research Institute (CSIR-NBRI)LucknowIndia
  2. 2.Academy of Scientific and Innovative Research (AcSIR)New DelhiIndia

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