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Small RNA-Mediated Defensive and Adaptive Responses in Plants

  • Afsar Raza Naqvi
  • Nirupam Roy Choudhury
  • Qazi Mohd. Rizwanul HaqEmail author
Chapter
Part of the Sustainable Agriculture Reviews book series (SARV, volume 7)

Abstract

Agriculture is the backbone of economy for most countries, especially the developing countries with high population density. However, the change in climate and its influence on the environment has led to low productivity of several staple crops that can be attributable to prevailing biotic and abiotic factors. In the long run, these factors are likely to have more adverse effects on the crop yield than what is currently being encountered. Therefore, scientists across the world develop strategies to tackle future problems leading to food insecurity. Plants are exposed to a variety of stresses under natural conditions. To encounter these challenges plants have efficiently evolved with several endogenous mechanisms to defend themselves against such harmful situations.

Small ribonucleic acids (sRNA) have recently been identified as critical molecules that regulate wide variety of biological phenomenon, both in plants and animals. Several lines of evidence demonstrates that small RNAs profiles changes rapidly in response to adverse stimuli. In certain cases, specific small RNAs were found to be associated with a particular stress, thus, indicating the direct involvement of small RNA-mediated pathways in plethora of stresses. We review here the advancements of small RNA biology, including microRNA and short-interfering RNA, and aspects related to their possible role in counter defense of biotic and abiotic stress responses. The review has been broadly classified into two sections describing role of small RNAs assigned in response to various biotic and abiotic stresses. The possible evidence of cross-talk among diverse range of stresses is also discussed. Future investigations may explore putative novel pathways downstream to this small RNA misexpression and consequently open avenues to design strategies to raise transgenic crops resistant to multiple stresses.

Keywords

Argonaute Cross-talk Dicer MiRNAs Plant defense responses SiRNAs Stress 

Notes

Acknowledgements

Financial assistance to ARN by CSIR, Government of India, is duly acknowledged.

References

  1. Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221. doi:10.1016/j.cell.2005.04.004PubMedCrossRefGoogle 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 18:1134–01151. doi:10.1105/tpc.105.040725PubMedCrossRefGoogle Scholar
  3. Anandalakshmi R, Pruss GJ, Ge X, Marathe R, Mallory AC, Smith HT, Vane VB (1998) A viral suppressor of gene silencing in plants. Proc Natl Acad Sci USA 95:13079–13084. doi:10.1073/pnas.1733874100PubMedCrossRefGoogle Scholar
  4. Andersson MG, Haasnoot PC, Xu N, Berenjian S, Berkhout B, Akusjarvi G (2005) Suppression of RNA interference by adenovirus virus-associated RNA. J Virol 79:9556–9565. doi:10.1128/JVI.79.15.9556–9565.2005PubMedCrossRefGoogle Scholar
  5. 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. doi:10.1105/tpc.016238PubMedCrossRefGoogle Scholar
  6. Aung K, Lin S, Wu C, Huang Y, Su C, Chiou T (2006) pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011. doi:10.1104/pp. 106.078063PubMedCrossRefGoogle Scholar
  7. Bao N, Lye KW, Barton MK (2004) MicroRNA binding sites in arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Dev Cell 7:653–662. doi:10.1016/j.devcel.2004.10.003PubMedCrossRefGoogle Scholar
  8. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297. doi:10.1016/S0092-8674(04)00045-5PubMedCrossRefGoogle Scholar
  9. Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits micro RNAs and short interfering RNAs. Proc Natl Acad Sci USA 102:11928–11933. doi:10.1073/pnas.0505461102PubMedCrossRefGoogle Scholar
  10. Bisaro DM (2006) Silencing suppression by geminivirus proteins. Virology 344:158–168. doi:10.1016/j.virol.2005.09.041PubMedCrossRefGoogle Scholar
  11. Blevins T, Rajeswaran R, Shivaprasad PV, Beknazariants D, Si-Ammour A, Park HS, Vazquez F, Robertson D, Meins FJ, Hohn T, Pooggin MM (2006) Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res 34:6233–6246. doi:10.1093/nar/gkl886PubMedCrossRefGoogle Scholar
  12. 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 130:1493–1504. doi:10.1242/10.1242/dev.00362PubMedCrossRefGoogle Scholar
  13. Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK (2005) Endogenous siRNAs derived from a pair of natural cisantisense transcripts regulate salt tolerance in Arabidopsis. Cell 123:1279–1291. doi:10.1016/j.cell.2005.11.035PubMedCrossRefGoogle Scholar
  14. Boualem A, Laporte P, Jovanovic M, Laffont C, Plet J, Combier JP, Niebel A, Crespi M, Frugier F (2008) MicroRNA 166 controls root and nodule development in Medicago trancatula. Plant J 54:876–887. doi:10.1111/j.1365-313X.2008.03448.xPubMedCrossRefGoogle Scholar
  15. Brigneti G, Voinnet O, Li WX, Ji LH, Ding SW, Baulcombe DC (1998) Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J 17:6739–6746. doi:10.1093/emboj/17.22.6739PubMedCrossRefGoogle Scholar
  16. 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 320:1185–1190. doi:10.1126/science.1159151PubMedCrossRefGoogle Scholar
  17. Chapman EJ, Prokhnevsky AI, Gopinath K, Dolja VV, Carrington JC (2004) Viral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step. Genes Dev 18:1179–1186. doi:10.1101/gad.1201204PubMedCrossRefGoogle Scholar
  18. Chellappan P, Vanitharani R, Fauquet CM (2005) MicroRNA-binding viral protein interferes with Arabidopsis development. Proc Natl Acad Sci USA 102:10381–10386. doi:10.1073/pnas.0504439102PubMedCrossRefGoogle Scholar
  19. Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025. doi:10.1126/science.1088060PubMedCrossRefGoogle Scholar
  20. Chen J, Li WX, Xie D, Peng JR, Ding SW (2004) Viral virulence protein suppresses RNA silencing-mediated defense but upregulates the role of microRNA in host gene expression. Plant Cell 16:1302–1313. doi:10.1105/tpc.018986PubMedCrossRefGoogle Scholar
  21. Cui X, Li G, Wang D, Hu D, Zhou X (2005) A Begomovirus DNA beta-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus. J Virol 79:10764–10775. doi:10.1128/JVI.79.16.10764-10775.2005PubMedCrossRefGoogle Scholar
  22. Deleris A, Gallego-Bartolome J, Bao J, Kasschau KD, Carrington JC, Voinnet O (2006) Hierarchial action and inhibition of plant Dicer-like proteins in antiviral defense. Science 303:68–71. doi:10.1126/science.1128214CrossRefGoogle Scholar
  23. Dunoyer P, Lecellier CH, Parizotto EA, Himber C, Voinnet O (2004) Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell 16:1235–1250. doi:10.1105/tpc.020719PubMedCrossRefGoogle Scholar
  24. Elbashir SM, Lendeckel W, Tuschl T (2001) RNA interference is mediated by 21- and 22-nucleotide RNAs. EMBO J 17:6739–6746. doi:10.1093/emboj/20.23.6877Google Scholar
  25. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13:1768–1774. doi:10.1016/S0960-9822(03)00718-8PubMedCrossRefGoogle Scholar
  26. Fagard M, Boutet S, Morel JB, Bellini C, Vaucheret H (2000) AGO1, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proc Natl Acad Sci USA 97:11650–11654. doi:10.1073/pnas.200217597PubMedCrossRefGoogle Scholar
  27. Fahlgren N, Montogomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16:939–944. doi:10.1016/j.cub.2006.03.065PubMedCrossRefGoogle Scholar
  28. Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL, Carrington JC (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE 2:e219. doi:10.1371/journal.pone.0000219PubMedCrossRefGoogle Scholar
  29. Felippes FF, Weigel D (2009) Triggering the formation of tasiRNAs in Arabidopsis thaliana: the role of microRNA miR173. EMBO Rep 10:264–270. doi:10.1038/embor.2008.247PubMedCrossRefGoogle Scholar
  30. Fenner BJ, Thiagarajan R, Chua HK, Kwang J (2006) Betanodavirus b2 is an RNA interference antagonist that facilitates intracellular viral RNA accumulation. J Virol 80:85–94. doi:10.1128/JVI.80.1.85-94.2006PubMedCrossRefGoogle Scholar
  31. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043. doi:10.1016/j.cub.2005.10.016PubMedCrossRefGoogle Scholar
  32. Gasciolli V, Mallory AC, Bartel DP, Vaucheret H (2005) Partially redundant functions of arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr Biol 15:1494–1500. doi:10.1016/j.cub.2005.07.024PubMedCrossRefGoogle Scholar
  33. Guo HS, Xie Q, Fie JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17:1376–1386. doi:10.1105/tpc.105.030841PubMedCrossRefGoogle Scholar
  34. Hamilton A, Baulcombe D (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952. doi:10.1126/science.286.5441.950PubMedCrossRefGoogle Scholar
  35. Han MH, 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. doi:10.1073/pnas.0307969100PubMedCrossRefGoogle Scholar
  36. 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 38:721–725. doi:10.1038/ng1804PubMedCrossRefGoogle Scholar
  37. Izquierdo J (1999) Biotechnology can help crop production to feed and increasing world population?: positive and negative aspects need to be balanced, a perspective from FAO. Presented at International Symposium on Plant Genetic Engineering, 6–10 Dec 1999, Havana (in print, Elsevier)Google Scholar
  38. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799. doi:10.1016/ j.molcel.2004.05.027PubMedCrossRefGoogle Scholar
  39. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P (2005) Modulation of hepatitis C virus RNA abundance by liver-specific MicroRNA. Science 309:1577–1581. doi:10.1126/science.1113329PubMedCrossRefGoogle Scholar
  40. Kasschau KD, Xie Z, Allen E, Llave C, Chapman EJ, Krizan KA, Carrington JC (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell 4:205–217. doi:10.1016/S1534-5807(03)00025-XPubMedCrossRefGoogle Scholar
  41. Katiyar-Agarwal S, Morgan R, Dahlbeck D, Borsani O, Villegas A Jr, Zhu JK, Staskawicz BJ, Jin H (2006) A pathogen-inducible endogenous siRNA in plant immunity. Proc Natl Acad Sci USA 103:18002–18007. doi:10.1073/pnas.0608258103PubMedCrossRefGoogle Scholar
  42. Katiyar-Agarwal S, Gao S, Vivian-Smith A, Jin H (2007) A novel class of bacteria-induced small RNAs in Arabidopsis. Genes Dev 21:3123–3134. doi:10.1101/gad.1595107PubMedCrossRefGoogle Scholar
  43. Khvorova A, Reynolds A, Jayasena SD (2003) Functional siRNAs and miRNAs exhibit strand bias. Cell 115:209–216. doi:10.1016/S0092-8674(03)00801-8PubMedCrossRefGoogle Scholar
  44. Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6:376–385. doi:10.1038/nrm1644PubMedCrossRefGoogle Scholar
  45. Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101:12753–12758. doi:10.1073/pnas.0403115101PubMedCrossRefGoogle Scholar
  46. Laufs P, Peaucelle A, Morin H, Traas J (2004) MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development 131:4311–4322. doi:10.1242/dev.01320PubMedCrossRefGoogle Scholar
  47. Lauter N, Kampani A, Carlson S, Goebel M, Moose SP (2005) MicroRNA172 down-regulates glossy15 to promote vegetative phase change in maize. Proc Natl Acad Sci USA 102:9412–9417. doi:10.1073/pnas.0503927102PubMedCrossRefGoogle Scholar
  48. Lecellier CH, Dunoyer P, Arar K, Lehmann-Che J, Eyquem S, Himber C, Saïb A, Voinnet O (2005) A cellular microRNA mediates antiviral defense in human cells. Science 308:557–560. doi:10.1126/science.1108784PubMedCrossRefGoogle Scholar
  49. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23:4051–4060. doi:10.1038/sj.emboj.7600385PubMedCrossRefGoogle Scholar
  50. Li F, Ding SW (2006) Virus counterdefense: diverse strategies for evading the RNA-Silencing immunity. Annu Rev Microbiol 60:503–531. doi:10.1146/annurev.micro.60.080805.142205PubMedCrossRefGoogle Scholar
  51. Li J, Yang Z, Yu B, Liu J, Chen X (2005) Methylation protects miRNAs and siRNAs from a 3-end uridylation activity in arabidopsis. Curr Biol 15:1501–1507. doi:10.1016/j.cub.2005.07.029PubMedCrossRefGoogle Scholar
  52. Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14:836–843. doi:10.1261/rna.895308PubMedCrossRefGoogle Scholar
  53. Lobbes D, Rallapalli G, Schmidt DD, Martin C, Clarke J (2006) SERRATE: a new player on the plant microRNA scene. EMBO Rep 7:1052–1058. doi:10.1038/sj.embor.7400806PubMedCrossRefGoogle Scholar
  54. Lu S, Cullen BR (2004) Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and microRNA biogenesis. J Virol 78:12868–12876. doi:10.1128/JVI.78.23.12868-12876.2004PubMedCrossRefGoogle Scholar
  55. Lu S, Sun Y-S, Shi R, Clark C, Li L, Chiang VL (2005) Novel and mechanical stressresponsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17:2186–2203. doi:10.1105/tpc.105.033456PubMedCrossRefGoogle Scholar
  56. Ma ZL, Yang HY, Wang R, Tian B (2004) Construct hairpin RNA to fight against rice dwarf virus. Acta Bot Sin 46:332–336Google Scholar
  57. Mallory AC, Reinhart BJ, Jones-Rhoades MW, Tang G, Zamore PD, Barton MK, Bartel DP (2004) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5 region. EMBO J 23:3356–3364. doi:10.1038/sj.emboj.7600340PubMedCrossRefGoogle Scholar
  58. Mallory AC, Hinze A, Tucker MR, Bouché N, Gasciolli V, Elmayan T, Lauressergues D, Jauvion V, Vaucheret H, Laux T (2009) Redundant and specific roles of the ARGONAUTE proteins AGO1 and ZLL in development and small RNA-directed gene silencing. PLoS Genet 5:e1000646. doi:10.1038/sj.emboj.7600340PubMedCrossRefGoogle Scholar
  59. Mette MF, Aufsatz W, van der Winden J, Matzke MA, Matzke AJ (2000) Transcriptional silencing and promoter methylation triggered by double stranded RNA. EMBO J 19:5194–5201. doi:10.1093/emboj/19.19.5194PubMedCrossRefGoogle Scholar
  60. Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H, Long C, Chen S, Hannon GJ, Qi Y (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5 terminal nucleotide. Cell 133:116–127. doi:10.1016/j.cell.2008.02.034PubMedCrossRefGoogle Scholar
  61. Mochizuki K, Gorovsky MA (2004) Conjugation-specific small RNAs in tetrahymena have predicted properties of scan (scn) RNAs involved in genome rearrangement. Genes Dev 18:2068–2073. doi:10.1101/gad.1219904PubMedCrossRefGoogle Scholar
  62. Moldovan D, Spriggs A, Yang J, Pogson BJ, Dennis ES, Wilson IW (2010) Hypoxia responsive miRNAs and trans-acting small interfering RNAs in Arabidopsis. J Exp Bot 61:165–177. doi:10.1093/jxb/erp296PubMedCrossRefGoogle Scholar
  63. Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, Alexander AL, Chapman EJ, Fahlgren N, Allen E, Carrington JC (2008) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133:128–141. doi:10.1016/j.cell.2008.02.033PubMedCrossRefGoogle Scholar
  64. Morel JB, Godon C, Mourrain P, Beclin C, Boutet S, Feuerbach F, Proux F, Vaucheret H (2002) Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in posttranscriptional gene silencing and virus resistance. Plant Cell 14:629–639. doi:10.1105/tpc.010358PubMedCrossRefGoogle Scholar
  65. Naqvi AR, Islam MN, Choudhury NR, Haq QM (2009) The fascinating world of RNA interference. Int J Biol Sci 5:97–117, PMCID: PMC2631224Google Scholar
  66. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JDG (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439. doi:10.1126/science.1126088PubMedCrossRefGoogle Scholar
  67. Navarro L, Jay F, Nomura K, He SY, Voinnet O (2008) Suppression of the microRNA pathway by bacterial effector proteins. Science 321:964–967. doi:10.1126/science.1159505PubMedCrossRefGoogle Scholar
  68. 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 24:1420–1428. doi:10.1038/nbt1255PubMedCrossRefGoogle Scholar
  69. Ortiz R (1998) Critical role of plant biotechnology for the genetic improvement of food crops-perspective for the next millennium. Elec J Biotechnol 1(3). http://www.ejb.ucv.cl/content/vol1/issue3/full/7/
  70. Pal-Bhadra M, Bhadra U, Birchler JA (2002) RNAi related mechanisms affect both transcriptional and post-transcriptional transgene silencing in Drosophila. Mol Cell 9:315–327. doi:10.1016/S1097-2765(02)00440-9PubMedCrossRefGoogle Scholar
  71. 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. doi:10.1073/pnas.0405570102PubMedCrossRefGoogle Scholar
  72. Pfeffer S, Zavolan M, Grässer FA, Chien M, Russo JJ, Ju J, John B, Enright AJ, Marks D, Sander C, Tuschl T (2004) Identification of virus-encoded microRNAs. Science 304:734–736. doi:10.1126/science.1096781PubMedCrossRefGoogle Scholar
  73. Pillai RS, Bhattacharyya SN, Artus CG, Zoller T, Cougot N, Basyuk E, Bertrand E, Filipowicz W (2005) Inhibition of translational initiation by Let-7 microRNA in human cells. Science 309:1573–1576. doi:10.1126/science.1115079PubMedCrossRefGoogle Scholar
  74. Qi Y, Zhong X, Itaya A, Ding B (2004) Dissecting RNA silencing in protoplasts uncovers novel effects of viral suppressors on the silencing pathway at the cellular level. Nucleic Acids Res 32:e179. doi:10.1093/nar/gnh180PubMedCrossRefGoogle Scholar
  75. Qi Y, He X, Wang XJ, Kohany O, Jurka J, Hannon GJ (2006) Distinct catalytic and non-catalytic role of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443:1008–1012. doi:10.1038/nature05198PubMedCrossRefGoogle Scholar
  76. Qu F, Ren T, Morris TJ (2003) The coat protein of turnip crinkle virus suppresses posttranscriptional gene silencing at an early initiation step. J Virol 77:511–522. doi:10.1128/JVI.77.1.511-522.2003PubMedCrossRefGoogle Scholar
  77. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse evolutionary fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20:3407–3425. doi:10.1101/gad.1476406PubMedCrossRefGoogle Scholar
  78. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133. doi:10.1105/tpc.105.039834PubMedCrossRefGoogle Scholar
  79. Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P (2008) The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol Biol 67:183–195. doi:10.1007/s11103-008-9310-zPubMedCrossRefGoogle Scholar
  80. Shibata S, Sasaki M, Miki T, Shimamoto A, Furuichi Y, Katahira J, Yoshihiro Y (2006) Exportin-5 orthologues are functionally divergent among species. Nucleic Acids Res 34:4711–4721. doi:10.1093/nar/gkl663PubMedCrossRefGoogle Scholar
  81. Silhavy D, Molnar A, Lucioli A, Szittya G, Hornyik C, Tavazza M, Burgyán J (2002) A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J 21:3070–3080. doi:10.1093/emboj/cdf312PubMedCrossRefGoogle Scholar
  82. 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 80:2429–2436. doi:10.1128/JVI.80.5.2429-2436.2006PubMedCrossRefGoogle Scholar
  83. Song L, Han MH, Lesicka J, Fedoroff N (2007) Arabidopsis primary microRNA processing proteins HYL1 and DCL1 define a nuclear body distinct from the cajal body. Proc Natl Acad Sci USA 104:5437–5442. doi:10.1073/pnas.0701061104PubMedCrossRefGoogle Scholar
  84. Sunkar R, Zhu JK (2004) Novel and stress regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019. doi:10.1105/tpc.104.022830PubMedCrossRefGoogle Scholar
  85. Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065. doi:10.1105/tpc.106.041673PubMedCrossRefGoogle Scholar
  86. Tagami Y, Inaba N, Kutsuna N, Kurihara Y, Watanabe Y (2007) Specific enrichment of miRNAs in Arabidopsis thaliana infected with tobacco mosaic virus. DNA Res 14:227–233. doi:10.1093/dnares/dsm022PubMedCrossRefGoogle Scholar
  87. Takeda A, Iwasaki S, Watanabe T, Utsumi M, Watanabe Y (2008) The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol 49:493–500. doi:10.1093/pcp/pcn043PubMedCrossRefGoogle Scholar
  88. Trinks D, Rajeswaran R, Shivaprasad PV, Akbergenov R, Oakeley EJ, Veluthambi K, Hohn T, Pooggin MM (2005) Suppression of RNA silencing by a geminivirus nuclear protein, AC2, correlates with transactivation of host genes. J Virol 79:2517–2527. doi:10.1128/JVI.79.4.2517-2527.2005PubMedCrossRefGoogle Scholar
  89. van Wezel R, Dong X, Liu H, Tien P, Stanley J, Hong Y (2002) Mutation of three cysteine residues in Tomato yellow leaf curl virus-China C2 protein causes dysfunction in pathogenesis and posttranscriptional gene-silencing suppression. Mol Plant Microbe Interact 15:203–208. doi:10.1094/MPMI.2002.15.3.203CrossRefGoogle Scholar
  90. Vanitharani R, Chen X (2008) Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science 321:1490–1492. doi:10.1126/science.1163728CrossRefGoogle Scholar
  91. Vanitharani R, Chellappan P, Pita JS, Fauquet CM (2004) Differential roles of AC2 and AC4 of cassava geminiviruses in mediating synergism and suppression of posttranscriptional gene silencing. J Virol 78:9487–9498. doi:10.1128/JVI.78.17.9487-9498.2004PubMedCrossRefGoogle Scholar
  92. Vaucheret H, Mallory AC, Bartel DP (2006) AGO1 homeostasis entails coexpression of MIR168 and AGO1 and preferential stabilization of miR168 by AGO1. Mol Cell 22:129–136. doi:10.1016/j.molcel.2006.03.011PubMedCrossRefGoogle Scholar
  93. Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, Mallory AC, Hilbert JL, Bartel DP, Crete P (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16:69–79. doi:10.1016/j.molcel.2004.09.028PubMedCrossRefGoogle Scholar
  94. Voinnet O (2005) Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 6:206–220. doi:10.1038/nrg1555PubMedCrossRefGoogle Scholar
  95. Voinnet O, Lederer C, Baulcombe DC (2000) A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103:157–167. doi:10.1016/S0092-8674(00)00095-7PubMedCrossRefGoogle Scholar
  96. Wang XJ, Gaasterland T, Chua NH (2005) Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana. Genome Biol 6:R30. doi:10.1186/gb-2005-6-4-r30PubMedCrossRefGoogle Scholar
  97. Wang H, Chua NH, Wang XJ (2006) Prediction of trans-antisense transcripts in Arabidopsis thaliana. Genome Biol 7:R92. doi:10.1186/gb-2006-7-10-r92PubMedCrossRefGoogle Scholar
  98. Xie Z, Kasschau KD, Carrington JC (2003) Negative feedback regulation of Dicer-like1 (DCL1) in arabidopsis by microRNA-guided mRNA degradation. Curr Biol 13:784–789. doi:10.1016/S0960-9822(03)00281-1PubMedCrossRefGoogle Scholar
  99. Xie Z, Allen E, Wilken A, Carrington JC (2005) Dicer-like 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc Natl Acad Sci USA 102:12984–12989. doi:10.1073/pnas.0506426102PubMedCrossRefGoogle Scholar
  100. Yoshikawa M, Peragine A, Park MY, Poethig RS (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19:2164–2175. doi:10.1101/gad.1352605PubMedCrossRefGoogle Scholar
  101. 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 307:932–935. doi:10.1126/science.1107130PubMedCrossRefGoogle Scholar
  102. Zheng X, Zhu J, Kapoor A, Zhu JK (2007) Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing. EMBO J 26:1691–1701. doi:10.1038/sj.emboj.7601603PubMedCrossRefGoogle Scholar
  103. Zhou X, Wang G, Sutoh K, Zhu JK, Zhang W (2008) Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochim Biophys Acta 1799:780–788. doi:10.1016/j.bbagrm.2008.04.005Google Scholar
  104. Zilberman D, Cao X, Jacobsen SE (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299:716–719. doi:10.1126/science.1079695PubMedCrossRefGoogle Scholar
  105. Zimmermann P, Hirsch-Hoffmann M, Henning L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632. doi:10.1104/pp. 104.046367CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Afsar Raza Naqvi
    • 1
    • 2
  • Nirupam Roy Choudhury
    • 2
  • Qazi Mohd. Rizwanul Haq
    • 1
    Email author
  1. 1.Department of BiosciencesJamia Millia Islamia (A Central University)New DelhiIndia
  2. 2.Plant Molecular Biology GroupInternational Centre for Genetic Engineering and BiotechnologyNew DelhiIndia

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