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Plant miRNAome and antiviral resistance: a retrospective view and prospective challenges

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Abstract

MicroRNAs (miRNAs) are small regulatory RNAs that play a defining role in post-transcriptional gene silencing of eukaryotes by either mRNA cleavage or translational inhibition. Plant miRNAs have been implicated in innumerable growth and developmental processes that extend beyond their ability to respond to biotic and abiotic stresses. Active in an organism’s immune defence response, host miRNAs display a propensity to target viral genomes. During viral invasion, these virus-targeting miRNAs can be identified by their altered expression. All the while, pathogenic viruses, as a result of their long-term interaction with plants, have been evolving viral suppressors of RNA silencing (VSRs), as well as viral-encoded miRNAs as a counter-defence strategy. However, the gene silencing attribute of miRNAs has been ingeniously manipulated to down-regulate the expression of any gene of interest, including VSRs, in artificial miRNA (amiRNA)-based transgenics. Since we currently have a better understanding of the intricacies of miRNA-mediated gene regulation in plant–virus interactions, the majority of miRNAs manipulated to confer antiviral resistance to date are in plants. This review will share the insights gained from the studies of plant-virus combat and from the endeavour to manipulate miRNAs, including prospective challenges in the context of the evolutionary dynamics of the viral genome. Next generation sequencing technologies and bioinformatics analysis will further delineate the molecular details of host–virus interactions. The need for appropriate environmental risk assessment principles specific to amiRNA-based virus resistance is also discussed.

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Abbreviations

amiRNA:

Artificial miRNA

DCL1:

Dicer-like 1

ERA:

Environmental risk assessment

EST:

Expressed sequence tag

hpRNA:

Hairpin RNA

ihpRNA:

Intron-spliced hairpin RNA

miRNA:

MicroRNA

NBS–LRR:

Nucleotide binding site–leucine-rich repeat

NGS:

Next generation sequencing

ncRNAs:

Non-coding RNAs

Pre-miRNA:

Precursor miRNA

Pri-miRNA:

Primary miRNA

RISC:

RNA-induced silencing complex

PTGS:

Post-transcriptional gene silencing

RNAi:

RNA interference

siRNA:

Small interfering RNA

SMRT:

Single molecule real time

tasiRNA:

Transacting siRNA

VSRs:

Viral suppressors of RNA silencing

VRTP:

Virus resistant transgenic plants

References

  1. B.J. Reinhart, E.G. Weinstein, M.W. Rhoades, B. Bartel, D.P. Bartel, MicroRNAs in plants. Genes Dev. 16, 1616–1626 (2002)

    CAS  PubMed  Google Scholar 

  2. X. Chen, J. Liu, Y. Cheng, D. Jia, HEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower. Development 129, 1085–1094 (2002)

    CAS  PubMed  Google Scholar 

  3. J.H. Clarke, D. Tack, K. Findlay, M. Van Montagu, M. Van Lijsebettens, The SERRATE locus controls the formation of the early juvenile leaves and phase length in Arabidopsis. Plant J. 20, 493–501 (1999)

    CAS  PubMed  Google Scholar 

  4. C. Lu, N. Fedoroff, A mutation in the arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell 12, 2351–2365 (2000)

    CAS  PubMed Central  PubMed  Google Scholar 

  5. M.D. Nodine, D.P. Bartel, MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev. 24, 2678–2692 (2010)

    CAS  PubMed  Google Scholar 

  6. J.F. Palatnik, E. Allen, X. Wu, C. Schommer, R. Schwab, J.C. Carrington, D. Weigel, Control of leaf morphogenesis by microRNAs. Nature 425, 257–263 (2003)

    CAS  PubMed  Google Scholar 

  7. Y. Wang, R. Blelloch, Cell cycle regulation by microRNAs in embryonic stem cells. Cancer Res. 69, 4093–4096 (2009)

    CAS  PubMed Central  PubMed  Google Scholar 

  8. G. Wu, M.Y. Park, S.R. Conway, J.W. Wang, D. Weigel, R.S. Poethig, The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138, 750–759 (2009)

    CAS  PubMed Central  PubMed  Google Scholar 

  9. A.A. Millar, J.V. Jacobsen, J.J. Ross, C.A. Helliwell, A.T. Poole, G. Scofield, J.B. Reid, F. Gubler, Seed dormancy and ABA metabolism in Arabidopsis and Barley: the role of ABA 8′-hydroxylase. Plant J. 45, 942–954 (2006)

    CAS  PubMed  Google Scholar 

  10. M.F. Wu, Q. Tian, J.W. Reed, Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133, 4211–4218 (2006)

    CAS  PubMed  Google Scholar 

  11. L. Navarro, P. Dunoyer, F. Jay, B. Arnold, N. Dharmasiri, M. Estelle, O. Voinnet, J.D. Jones, A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436–439 (2006)

    CAS  PubMed  Google Scholar 

  12. R. Sunkar, J. Zhu, Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16, 2001–2019 (2004)

    CAS  PubMed Central  PubMed  Google Scholar 

  13. N. Sanan-Mishra, V. Kumar, S.K. Sopory, S.K. Mukherjee, Cloning and validation of novel miRNA from basmati rice indicates cross-talk between abiotic and biotic stresses. Mol. Genet. Genomics 282, 463–474 (2009)

    CAS  PubMed  Google Scholar 

  14. J.C. Sanford, S.A. Johnston, The concept of pathogen derived resistance. J. Theor. Biol. 113, 395–405 (1985)

    Google Scholar 

  15. P.P. Abel, R.S. Nelson, B. De, N. Hoffmann, S.G. Rogers, R.T. Fraley, R.N. Beachy, Delay of disease development in transgenic plants that express the Tobacco mosaic virus coat protein gene. Science 232, 738–743 (1986)

    CAS  PubMed  Google Scholar 

  16. J.A. Lindbo, L. Silva-Rosales, W.M. Proebsting, W.G. Dougherty, Induction of a highly specific antiviral state in transgenic plants: implications for regulation of gene expression and virus resistance. Plant Cell 5, 1749–1759 (1993)

    CAS  PubMed Central  PubMed  Google Scholar 

  17. M. Prins, P. De Haan, R. Luyten, M. Van Veller, M.Q.J.M. Van Grinsven, R. Goldbach, Broad resistance to tospoviruses in transgenic plants by expressing three tospoviral nucleoprotein gene sequences. Mol. Plant Microbe Interact. 8, 85–91 (1995)

    CAS  PubMed  Google Scholar 

  18. A.L. Jones, I.E. Johansen, S.J. Bean, I. Bach, A.J. Maule, Specificity of resistance to pea seed-borne mosaic potyvirus in transgenic peas expressing the viral replicase (NIb) gene. J. Gen. Virol. 79, 3129–3137 (1998)

    CAS  PubMed  Google Scholar 

  19. F. Tenllado, J.R. Dıaz-Ruız, Complete resistance to pepper mild mottle tobamovirus mediated by viral replicase sequences partially depends on transgene homozygosity and is based on a gene silencing mechanism. Transgenic Res. 8, 83–93 (1999)

    CAS  Google Scholar 

  20. K. Kalantidis, S. Psaradakis, M. Tabler, M. Tsagris, The occurrence of CMV specific short RNAs in transgenic tobacco expressing virus-derived double stranded RNA is indicative of resistance to the virus. Mol. Plant Microbe Interact. 15, 826–833 (2002)

    CAS  PubMed  Google Scholar 

  21. S.W. Ding, O. Voinnet, Antiviral immunity directed by small RNAs. Cell 130, 413–426 (2007)

    CAS  PubMed Central  PubMed  Google Scholar 

  22. R. Vanitharani, P. Chellappan, C.M. Fauquet, Short interfering RNA-mediated interference of gene expression and viral DNA accumulation in cultured plant cells. Proc. Natl. Acad. Sci. U.S.A. 100, 9632–9636 (2003)

    CAS  PubMed Central  PubMed  Google Scholar 

  23. Y. Fang, D.L. Spector, Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr. Biol. 17, 818–823 (2007)

    CAS  PubMed Central  PubMed  Google Scholar 

  24. Y. Lee, M. Kim, J. Han, K.H. Yeom, S. Lee, S.H. Baek, V.N. Kim, MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23, 4051–4060 (2004)

    CAS  PubMed  Google Scholar 

  25. Z. Xie, E. Allen, N. Fahlgren, A. Calamar, S.A. Givan, J.C. Carrington, Expression of Arabidopsis MIRNA genes. Plant Physiol. 138, 2145–2154 (2005)

    CAS  PubMed Central  PubMed  Google Scholar 

  26. B. Yu, L. Bi, B. Zheng, L. Ji, D. Chevalier, M. Agarwal, V. Ramachandran, W. Li, T. Lagrange, J.C. Walker, X. Chen, The FHA domain proteins DAWDLE in Arabidopsis and SNIP1 in humans act in small RNA biogenesis. Proc. Natl. Acad. Sci. U.S.A. 105, 10073–10078 (2008)

    CAS  PubMed Central  PubMed  Google Scholar 

  27. Y. Kurihara, Y. Watanabe, Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc. Natl. Acad. Sci. U.S.A. 101, 12753–12758 (2004)

    CAS  PubMed Central  PubMed  Google Scholar 

  28. M.H. Han, S. Goud, L. Song, N. Fedoroff, The Arabidopsis double stranded RNA-binding protein HYL1 plays a role in microRNA mediated gene regulation. Proc. Natl. Acad. Sci. U.S.A. 101, 1093–1098 (2004)

    CAS  PubMed Central  PubMed  Google Scholar 

  29. Y. Kurihara, Y. Takashi, Y. Watanabe, The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA 12, 206–212 (2006)

    CAS  PubMed  Google Scholar 

  30. W. Park, J. Li, R. Song, J. Messing, X. Chen, CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol. 12, 484–1495 (2002)

    Google Scholar 

  31. K.M. Bollman, M.J. Aukerman, M.Y. Park, C. Hunter, T.Z. Berardini, R.S. Poethig, HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis. Development 130, 1493–1504 (2003)

    CAS  PubMed  Google Scholar 

  32. D.P. Bartel, MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297 (2004)

    CAS  PubMed  Google Scholar 

  33. P. Brodersen, L. Sakvarelidze-Achard, M. Bruun-Rasmussen, P. Dunoyer, Y.Y. Yamamoto, L. Sieburth, O. Voinnet, Widespread translational inhibition by plant miRNAs and siRNAs. Science 20, 1185–1190 (2008)

    Google Scholar 

  34. M.J. Aukerman, H. Sakai, Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15, 2730–2741 (2003)

    CAS  PubMed Central  PubMed  Google Scholar 

  35. B.D. Pant, M. Musialak-Lange, P. Nuc, P. May, A. Buhtz, J. Kehr, D. Walther, W.R. Scheible, Identification of nutrient responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol. 150, 1541–1555 (2009)

    PubMed Central  PubMed  Google Scholar 

  36. R. Pacheco, A. García-Marcos, D. Barajas, J. Martiáñez, F. Tenllado, PVX–potyvirus synergistic infections differentially alter microRNA accumulation in Nicotiana benthamiana. Virus Res. 165, 231–235 (2012)

    CAS  PubMed  Google Scholar 

  37. R.C. Lee, R.L. Feinbaum, V. Ambros, The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843–854 (1993)

    CAS  PubMed  Google Scholar 

  38. C. Llave, MicroRNAs: more than a role in plant development? Mol. Plant Pathol. 5, 361–366 (2004)

    CAS  PubMed  Google Scholar 

  39. C.H. Lecellier, P. Dunoyer, K. Arar, C.J. Lehmann, S. Eyquem, C. Himber, A. Saïb, O. Voinnet, A cellular microRNA mediates antiviral defense in human cells. Science 308, 557–560 (2005)

    CAS  PubMed  Google Scholar 

  40. C. Simon-Mateo, J.A. Garcia, MicroRNA-guided processing impairs Plum pox virus replication, but the virus readily evolves to escape this silencing mechanism. J. Virol. 80, 2429–2436 (2006)

    CAS  PubMed Central  PubMed  Google Scholar 

  41. A.R. Naqvi, Q.M. Haq, S.K. Mukherjee, 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 (2010)

    PubMed Central  PubMed  Google Scholar 

  42. I. Amin, L.P. Basavaprabhu, R.W. Briddon, S. Mansoo, C.M. Fauquet, Common set of developmental miRNAs are upregulated in Nicotiana benthamiana by diverse begomoviruses. Virol. J. 8, 143 (2011)

    CAS  PubMed Central  PubMed  Google Scholar 

  43. A. Pérez-Quintero, R. Neme, A. Zapata, C. López, Plant miRNAs and their role in defense against viruses: a bioinformatics approach. BMC Plant Biol. 10, 138 (2010)

    PubMed Central  PubMed  Google Scholar 

  44. I.M. Ehrenreich, M.D. Purugganan, Sequence variation of microRNAs and their binding sites in Arabidopsis. Plant Physiol. 146, 1974–1982 (2008)

    CAS  PubMed Central  PubMed  Google Scholar 

  45. J. Zhai, J. Dong-Hoon, D.P. Emanuele, S. Park, D.R. Benjamin, L. Yupeng, A.J. González, Z. Yan, L.K. Sherry, A.G. Michael, S.A. Jackson, G. Stacey, D.R. Cook, P.J. Green, S. Janine, B.C. Meyers, MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev. 25, 2540–2553 (2011)

    CAS  PubMed  Google Scholar 

  46. F. Li, D. Pignatta, C. Bendix, J.O. Brunkard, M.M. Cohn, J. Tung, H. Sun, P. Kumar, B. Baker, MicroRNA regulation of plant innate immune receptors. Proc. Natl. Acad. Sci. U.S.A. 109, 1790–1795 (2012)

    CAS  PubMed Central  PubMed  Google Scholar 

  47. P.V. Shivaprasad, H.M. Chen, K. Patel, D.M. Bond, B.A.C.M. Santos, D.C. Baulcombe, A microRNA superfamily regulates nucleotide binding site–leucine-rich repeats and other mRNAs. Plant Cell 24, 859–874 (2012)

    CAS  PubMed Central  PubMed  Google Scholar 

  48. V.S. Mahajan, A. Drake, J. Chen, Virus-specific host miRNAs: antiviral defenses or promoters of persistent infection? Trends Immunol. 30, 1–7 (2009)

    CAS  PubMed Central  PubMed  Google Scholar 

  49. X. Wang, J. Zhang, F. Li, G. Jin, H. Tao, X. Zhang, L. Yanda, MicroRNA identification based on sequence and structure alignment. Bioinformatics 21(18), 3610–3614 (2005)

    CAS  PubMed  Google Scholar 

  50. M. Zuker, Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31(13), 3406–3415 (2003)

    CAS  PubMed Central  PubMed  Google Scholar 

  51. M. Rehmsmeier, P. Steffen, M. Hochsmann, R. Giegerich, Fast and effective prediction of microRNA/target duplexes. RNA 10(10), 1507–1517 (2004)

    CAS  PubMed  Google Scholar 

  52. J. Kruger, M. Rehmsmeier, RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Res. 34(2), 451–454 (2006)

    Google Scholar 

  53. O.L.A. SaeTrom, O.J. Snove, P.A.L. SaeTrom, Weighted sequence motifs as an improved seeding step in microRNA target prediction algorithms. RNA 11(7), 995–1003 (2005)

    CAS  PubMed  Google Scholar 

  54. K. Sung-Kyu, N. Jin-Wu, L. Wha-Jin, Z. Byoung-Tak, A Kernel method for microRNA target prediction using sensible data and position-based features in Proceedings of the 2005 IEEE Symposium on Computational Intelligence in Bioinformatics and Computational Biology (CIBCB, La Jolla, 2005), pp 46–52

  55. K.C. Miranda, T. Huynh, Y. Tay, Y.S. Ang, W.L. Tam, A.M. Thomson, B. Lim, I. Rigoutsos, A pattern-based method for the identification of microRNA binding sites and their corresponding heteroduplexes. Cell 126(6), 1203–1217 (2006)

    CAS  PubMed  Google Scholar 

  56. F. Xiao, Z. Zuo, G. Cai, S. Kang, X. Gao, T. Li, miRecords: an integrated resource for microRNA–target interactions. Nucleic Acids Res. 37(Suppl 1), 105–110 (2009)

    CAS  Google Scholar 

  57. Q. Niu, S. Lin, J. Reyes, K. Chen, H. Wu, S. Ye, N. Chua, Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat. Biotechnol. 24(11), 1420–1427 (2006)

    CAS  PubMed  Google Scholar 

  58. J. Qu, J. Ye, R. Fang, Artificial microRNA-mediated virus resistance in plants. J. Virol. 81, 6690–6699 (2007)

    CAS  PubMed Central  PubMed  Google Scholar 

  59. M. Fahim, P.J. Larkin, Designing effective amiRNA and multimeric amiRNA against plant viruses. Methods Mol. Biol. 942, 357–377 (2013)

    CAS  PubMed  Google Scholar 

  60. N.S. Jelly, P. Schellenbaum, B. Walter, P. Maillot, Transient expression of artificial microRNAs targeting Grapevine fanleaf virus and evidence for RNA silencing in grapevine somatic embryos. Transgenic Res. 6, 1319–1327 (2012)

    Google Scholar 

  61. P. Palukaitis, S. MacFarlane, Viral counter-defense molecules, in Natural Resistance Mechanisms of Plants to Viruses, ed. by G. Loebenstein, J.P. Carr (Springer, Netherlands, 2006), pp. 165–185

    Google Scholar 

  62. O. Voinnet, Induction and suppression of RNA silencing: insights from viral infections. Nat. Rev. Genet. 6, 206–220 (2005)

    CAS  PubMed  Google Scholar 

  63. R. Anandalakshmi, G.J. Pruss, X. Ge, R. Marathe, A.C. Mallory, T.H. Smith, V.B. Vance, A viral suppressor of gene silencing in plants. Proc. Natl. Acad. Sci. U.S.A. 95, 13079–13084 (1998)

    CAS  PubMed Central  PubMed  Google Scholar 

  64. G. Brigneti, O. Voinnet, W.X. Li, L.H. Ji, S.W. Ding, D.C. Baulcombe, Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J. 17, 6739–6746 (1998)

    CAS  PubMed  Google Scholar 

  65. K.D. Kasschau, J.C. Carrington, A counter defensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell 95, 461–470 (1998)

    CAS  PubMed  Google Scholar 

  66. O. Voinnet, Y.M. Pinto, D.C. Baulcombe, Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc. Natl. Acad. Sci. U.S.A. 96, 14147–14152 (1999)

    CAS  PubMed Central  PubMed  Google Scholar 

  67. D.M. Bisaro, Silencing suppression by geminivirus proteins. Virology 344, 158–168 (2006)

    CAS  PubMed  Google Scholar 

  68. Z. Merai, Z. Kerényi, S. Kertész, M. Magna, L. Lakatos, D. Silvahy, Double-stranded RNA binding may be a general plant RNA viral strategy to suppress RNA silencing. J. Virol. 80, 5747–5756 (2006)

    CAS  PubMed Central  PubMed  Google Scholar 

  69. A.J. Love, J. Laird, J. Holt, A.J. Hamilton, A. Sadanandom, J.J. Milner, Cauliflower mosaic virus protein P6 is a suppressor of RNA silencing. J. Gen. Virol. 88, 3439–3444 (2007)

    CAS  PubMed  Google Scholar 

  70. D. Silhavy, A. Molnár, A. Lucioli, G. Szittya, C. Hornyik, M. Tavazza, J. Burgyán, A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J. 21, 3070–3080 (2002)

    CAS  PubMed  Google Scholar 

  71. L. Lakatos, T. Csorba, V. Pantaleo, E.J. Chapman, J.C. Carrington, Y.P. Liu, V.V. Dolja, L.F. Calvino, J.J. López-Moya, J. Burgyán, Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO J. 25, 2768–2780 (2006)

    CAS  PubMed  Google Scholar 

  72. T. Csorba, A. Bovi, T. Dalmay, J. Burgyan, The p122 subunit of Tobacco mosaic virus replicase is a potent silencing suppressor and compromises both small interfering RNA- and microRNA-mediated pathways. J. Virol. 81, 11768–11780 (2007)

    CAS  PubMed Central  PubMed  Google Scholar 

  73. X. Zhang, Y.R. Yuan, Y. Pei, S.S. Lin, T. Tuschl, D.J. Patel, N.H. Chua, Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev. 20, 3255–3268 (2006)

    CAS  PubMed  Google Scholar 

  74. H.S. Guo, S.W. Ding, A viral protein inhibits the long range signaling activity of the gene silencing signal. EMBO J. 21, 398–407 (2002)

    CAS  PubMed  Google Scholar 

  75. P. Dunoyer, C.A. Brosnan, G. Schott, Y. Wang, F. Jay, A. Alioua, C. Himber, O. Voinnet, An endogenous, systemic RNAi pathway in plants. EMBO J. 29, 1699–1712 (2010)

    CAS  PubMed  Google Scholar 

  76. H.A. Ebhardt, E.P. Thi, M.B. Wang, P.J. Unrau, Extensive 3′ modification of plant small RNAs is modulated by helper component-proteinase expression. Proc. Natl. Acad. Sci. U.S.A. 102, 13398–13403 (2005)

    CAS  PubMed Central  PubMed  Google Scholar 

  77. H. Vogler, R. Akbergenov, P.V. Shivaprasad, V. Dang, M. Fasler, K. Myoung-Ok, S. Zhanybekova, T. Hohn, M. Heinlein, Modification of small RNAs associated with suppression of RNA silencing by tobamovirus replicase protein. J. Virol. 81, 10379–10388 (2007)

    CAS  PubMed Central  PubMed  Google Scholar 

  78. B. Yu, E.J. Chapman, Z. Yang, J.C. Carrington, X. Chen, Transgenically expressed viral RNA silencing suppressors interfere with microRNA methylation in Arabidopsis. FEBS Lett. 580, 3117–3120 (2006)

    CAS  PubMed  Google Scholar 

  79. J. Azevedo, D. Garcia, D. Pontier, S. Ohnesorge, A. Yu, S. Garcia, L. Braun, M. Bergdoll, M.A. Hakimi, T. Lagrange, O. Voinnet, Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen-encoded GW repeat protein. Genes Dev. 24, 904–915 (2010)

    CAS  PubMed  Google Scholar 

  80. A. Giner, L. Lakatos, M. Garcia-Chapa, J.J. Lopez-Moya, J. Burgyan, Viral protein inhibits RISC activity by argonaute binding through conserved WG/GW motifs. PLoS Pathog. 6, e1000996 (2010)

    PubMed Central  PubMed  Google Scholar 

  81. J.A. Diaz-Pendon, F. Li, W.X. Li, S.W. Ding, Suppression of antiviral silencing by cucumber mosaic virus 2b protein in Arabidopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. Plant Cell 19, 2053–2063 (2007)

    CAS  PubMed Central  PubMed  Google Scholar 

  82. H. Wang, K.J. Buckley, X. Yang, R.C. Buchmann, D.M. Bisaro, Adenosine kinase inhibition and suppression of RNA silencing by geminivirus AL2 and L2 proteins. J. Virol. 79, 7410–7418 (2005)

    CAS  PubMed Central  PubMed  Google Scholar 

  83. A. Kanazawa, J.-I. Inaba, H. Shimura, S. Otagaki, S. Tsukahara, A. Matsuzawa, B.M. Kim, K. Goto, C. Masuta, Virus-mediated efficient induction of epigenetic modifications of endogenous genes with phenotypic changes in plants. Plant J. 65, 156–168 (2011)

    CAS  PubMed  Google Scholar 

  84. E.J. Chapman, A.I. Prokhnevsky, K. Gopinath, V.V. Dolja, J.C. Carrington, Viral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step. Genes Dev. 18, 1179–1186 (2004)

    CAS  PubMed  Google Scholar 

  85. P. Chellappan, R. Vanitharani, F. Ogbe, C.M. Fauquet, Effect of temperature on geminivirus-induced RNA silencing in plants. Plant Physiol. 138, 1828–1841 (2005)

    CAS  PubMed Central  PubMed  Google Scholar 

  86. J. Chen, W.L. Xiang, D. Xie, J.R. Peng, S.W. Ding, Viral virulence protein suppresses RNA silencing-mediated defense but upregulates the role of microRNA in host gene expression. Plant Cell 16, 1302–1313 (2004)

    CAS  PubMed Central  PubMed  Google Scholar 

  87. P. Dunoyer, C.H. Lecellier, E.A. Parizotto, C. Himber, O. Voinnet, Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell 16, 1235–1250 (2004)

    CAS  PubMed Central  PubMed  Google Scholar 

  88. D. Bortolamiol, M. Pazhouhandeh, K. Marrocco, P. Genschik, V. Ziegler-Graff, The Polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr. Biol. 17, 1615–1621 (2007)

    CAS  PubMed  Google Scholar 

  89. E. Varallyay, A. Válóczi, A. Agyi, J. Burgyán, Z. Havelda, Plant virus-mediated induction of miR168 is associated with repression of ARGONAUTE1 accumulation. EMBO J. 29, 3507–3519 (2010)

    CAS  PubMed  Google Scholar 

  90. M. Lewsey, F.C. Robertson, T. Canto, P. Palukaitis, J.P. Carr, Selective targeting of miRNA-regulated plant development by a viral counter-silencing protein. Plant J. 50, 240–252 (2007)

    CAS  PubMed  Google Scholar 

  91. M.W. Endres, B.D. Gregory, Z. Gao, A.W. Foreman, S. Mlotshwa, G. Xin, J.P. Gail, R.E. Joseph, H.B. Lewis, V. Vicki, Two plant viral suppressors of silencing require the ethylene-inducible host transcription factor RAV2 to block RNA silencing. PLoS Pathog. 6, e1000729 (2010)

    PubMed Central  PubMed  Google Scholar 

  92. G. Schott, A. Mari-Ordonez, C. Himber, A. Alioua, O. Voinnet, P. Dunoyer, Differential effects of viral silencing suppressors on siRNA and miRNA loading support the existence of two distinct cellular pools of ARGONAUTE1. EMBO J. 31(11), 2553–2565 (2012)

    CAS  PubMed  Google Scholar 

  93. C.S. Sullivan, D. Ganem, MicroRNAs and viral infection. Mol. Cell 20, 3–7 (2005)

    CAS  PubMed  Google Scholar 

  94. S. Pfeffer, M. Zavolan, F.A. Gra¨sser, M. Chien, J.J. Russo, J. Ju, B. John, A.J. Enright, D. Marks, C. Sander, T. Tuschl, Identification of virus-encoded microRNAs. Science 304(5671), 734–736 (2004)

    CAS  PubMed  Google Scholar 

  95. R.L. Skalsky, B.R. Cullen, Viruses, microRNAs, and host interactions. Annu. Rev. Microbiol. 64, 123–141 (2010)

    CAS  PubMed Central  PubMed  Google Scholar 

  96. R.P. Kincaid, J.M. Burke, C.S. Sullivan, RNA virus microRNA that mimics a B-cell oncomiR. Proc. Natl. Acad. Sci. U.S.A. 109, 3077–3082 (2012)

    CAS  PubMed Central  PubMed  Google Scholar 

  97. R.P. Kincaid, C.S. Sullivan, Virus-encoded microRNAs: an overview and a look to the future. PLoS Pathog. 8(12), e1003018 (2012)

    CAS  PubMed Central  PubMed  Google Scholar 

  98. J.W. Carl, J. Trgovcich, S. Hannenhalli, Widespread evidence of viral miRNAs targeting host pathways. BMC Bioinform. 14(Suppl 2), S3 (2013)

    CAS  Google Scholar 

  99. Z.A. Klase, G.C. Sampey, F. Kashanchi, Retrovirus infected cells contain viral microRNAs. Retrovirology 10, 15 (2013)

    CAS  PubMed  Google Scholar 

  100. I. Shazia, Role of viral and host MicroRNAs in plant virus interaction, Ph.D. Thesis, School of Biological Sciences, The University of Queensland, 2010

  101. J.P. Alvarez, I. Pekker, A. Goldschimt, E. Plum, Z. Amsellam, Y. Eshed, Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18, 1134–1151 (2006)

    CAS  PubMed Central  PubMed  Google Scholar 

  102. R. Schwab, S. Ossowski, M. Riester, N. Warthmann, D. Weigel, Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18, 1121–1133 (2006)

    CAS  PubMed Central  PubMed  Google Scholar 

  103. E.A. Parizotto, P. Dunoyer, N. Rahm, C. Himber, O. Voinnet, In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes Dev. 18, 2237–2242 (2004)

    CAS  PubMed  Google Scholar 

  104. H. Vaucheret, F. Vazquez, P. Crete, D.P. Bartel, 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 (2004)

    CAS  PubMed  Google Scholar 

  105. R. Schwab, S. Ossowski, N. Warthman, D. Weigel, Directed gene silencing with artificial microRNAs, in Plant MicroRNAs, Methods in Molecular Biology, ed. by B.C. Meyers, P.J. Green (Humana Press, Clifton, 2010), pp. 71–89

    Google Scholar 

  106. A.C. Mallory, B.J. Reinhart, M.W. Jones-Rhoades, G. Tang, P.D. Zamore, M.K. Barton, D.P. Bartel, MicroRNA control of PHABULOSA in leaf development, importance of pairing to the microRNA 59 region. EMBO J. 23, 3356–3364 (2004)

    CAS  PubMed  Google Scholar 

  107. A. Reynolds, D. Leake, Q. Boese, S. Scaringe, W.S. Marshall, A. Khvorova, Rational siRNA design for RNA interference. Nat. Biotechnol. 22, 326–330 (2004)

    CAS  PubMed  Google Scholar 

  108. M. Kertesz, N. Lovino, U. Unnerstall, U. Gaul, E. Segal, The role of site accessibility in microRNA target recognition. Nat. Genet. 39, 1278–1284 (2007)

    CAS  PubMed  Google Scholar 

  109. N. Warthmann, H. Chen, S. Ossowski, D. Weigel, P. Herve, Highly specific gene silencing by artificial miRNAs in rice. PLoS One 3, e1829 (2008)

    PubMed Central  PubMed  Google Scholar 

  110. C.G. Duan, C.H. Wang, R.X. Fang, H.S. Guo, Artificial microRNAs highly accessible to targets confer efficient virus resistance in plants. J. Virol. 82, 11084–11095 (2008)

    CAS  PubMed Central  PubMed  Google Scholar 

  111. H. Yan, X. Deng, Y. Cao, J. Huang, L. Ma, B. Zhao, A novel approach for the construction of plant amiRNA expression vectors. J. Biotechnol. 151(1), 9–14 (2011)

    CAS  PubMed  Google Scholar 

  112. B.N. Chung, T. Canto, P. Palukaitis, Stability of recombinant plant viruses containing genes of unrelated plant viruses. J. Gen. Virol. 88, 1347–1355 (2007)

    CAS  PubMed  Google Scholar 

  113. R. Yi, Y. Qin, I.G. Macara, B.R. Cullen, Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 17, 3011–3016 (2003)

    CAS  PubMed  Google Scholar 

  114. S. Lin, H. Wu, S. Elena, K. Chen, Q. Niu, S. Ye, C. Chen, N.H. Chua, Molecular evolution of a viral non-coding sequence under the selective pressure of amiRNA-mediated silencing. PLoS Pathog. 5(2), e1000312 (2009)

    PubMed Central  PubMed  Google Scholar 

  115. G. Lafforgue, F. Martínez, S. Josep, I. Francisca, N. Qi-Wen, L. Shih-Shun, V.S. Ricard, C. Nam-Hai, D. José-Antonio Don, F.E. Santiago, Tempo and mode of plant RNA virus escape from RNA interference-mediated resistance. J. Virol. 85(19), 9686 (2011)

    CAS  PubMed Central  PubMed  Google Scholar 

  116. F. Martínez, G. Lafforgue, M.J. Morelli, F. González-Candelas-, N.H. Chua, J.A. Daro`s, S.F. Elena, Ultradeep sequencing analysis of population dynamics of virus escape mutants in RNAi mediated resistant plants. Mol. Biol. Evol. 29(11), 3297–3307 (2012)

    PubMed  Google Scholar 

  117. A.R. Naqvi, N.R. Choudhury, S.K. Mukherjee, Q.M.R. Haq, In silico analysis reveals that several tomato microRNA/microRNA* sequences exhibit propensity to bind to tomato leaf curl virus (ToLCV) associated genomes and most of their encoded open reading frames (ORFs). Plant Physiol. Biochem. 49(1), 13–17 (2011)

    CAS  PubMed  Google Scholar 

  118. Y. Lu, Q. Gan, X. Chi, S. Qin, Roles of microRNA in plant defense and virus offense interaction. Plant Cell Rep. 27, 1571–1579 (2008)

    CAS  PubMed  Google Scholar 

  119. X. Zhang, H. Li, J. Zhang, C. Zhang, P. Gong, K. Ziaf, F. Xiao, Z. Ye, Expression of artificial microRNAs in tomato confers efficient and stable virus resistance in a cell-autonomous manner. Transgenic Res. 3, 1–13 (2011)

    CAS  Google Scholar 

  120. R. Schwab, O. Voinnet, RNA silencing amplification in plants: size matters. Proc. Natl. Acad. Sci. U.S.A. 107(34), 14945–14946 (2010)

    CAS  PubMed Central  PubMed  Google Scholar 

  121. J.M. Franco-Zorrilla, A. Valli, M. Todesco, I. Mateos, M.I. Puga, I. Rubio-Somoza, A. Leyva, D. Weigel, J.A. García, J. Paz-Ares, Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39(8), 1033–1037 (2007)

    CAS  PubMed  Google Scholar 

  122. Z. Deng, Y. Xiangling, F. Ling, J.R. Zina, B.B. Yang, Misprocessing and functional arrest of microRNAs by miR-Pirate: roles of miR-378 and miR-17. Biochem. J. 450, 375–386 (2013)

    CAS  PubMed  Google Scholar 

  123. J.P. Zhao, X.L. Jiang, B.Y. Zhang, X.H. Su, Involvement of microRNA-mediated gene expression regulation in the pathological development of stem canker disease in Populus trichocarpa. PLoS One 7(9), e44968 (2012)

    CAS  PubMed Central  PubMed  Google Scholar 

  124. C.C. Pritchard, H.H. Cheng, T. Muneesh, MicroRNA profiling: approaches and considerations. Nat. Rev. Genet. 13, 358–369 (2012)

    CAS  PubMed  Google Scholar 

  125. A. Jha, R. Shankar, Employing machine learning for reliable miRNA target identification in plants. BMC Genom. 12, 636 (2011)

    CAS  Google Scholar 

  126. P.H. Williams, R. Eyles, G. Weiller, Plant microRNA prediction by supervised machine learning using C5.0 decision trees. J. Nucleic Acids, Article ID 652979 (2012)

  127. M. Fahim, A.M. Anthony, C.C. Wood, P.J. Larkin, Resistance to wheat streak mosaic virus generated by expression of an artificial polycistronic microRNA in wheat. Plant Biotechnol. J. 10(2), 150–163 (2012)

    CAS  PubMed  Google Scholar 

  128. X. Lin, X. Ruan, M.G. Anderson, J.A. McDowell, P.E. Kroeger, S.W. Fesik et al., siRNA-mediated off-target gene silencing triggered by a 7 nt complementation. Nucleic Acids Res. 33, 4527–4535 (2005)

    CAS  PubMed Central  PubMed  Google Scholar 

  129. S. Praveen, S.V. Ramesh, A.K. Mishra, V. Koundal, P. Palukaitis, Silencing potential of viral derived RNAi constructs in tomato leaf curl virus-AC4 gene suppression in tomato. Transgenic Res. 19, 45–55 (2010)

    CAS  PubMed  Google Scholar 

  130. L. Zhang, D. Hou, X. Chen, D. Li, L. Zhu, Y. Zhang, J. Li, Z. Bian, X. Liang, X. Cai, Y. Yin, C. Wang, T. Zhang, D. Zhu, D. Zhang, J. Xu, Q. Chen, Y. Ba, J. Liu, Q. Wang, J. Chen, J. Wang, M. Wang, Q. Zhang, J. Zhang, K. Zen, C.Y. Zhang, Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Res. 22, 107–126 (2012)

    CAS  PubMed  Google Scholar 

  131. T. Ai, L. Zhang, Z. Gao, C.X. Zhu, X. Guo, Highly efficient virus resistance mediated by artificial microRNAs that target the suppressor of PVX and PVY in plants. Plant Biol. 13(2), 304–316 (2011)

    CAS  PubMed  Google Scholar 

  132. Y.J. Kung, S.S. Lin, Y.L. Huang, T.C. Chen, S.S. Harish, N.H. Chua, S.D. Yeh, 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(3), 303–317 (2012)

    CAS  PubMed  Google Scholar 

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Acknowledgments

The authors express their gratitude to Dr. S.K. Srivastava, Director, Directorate of Soybean Research, Indore, for providing amenities during the study. The work is an integral part of the Directorate’s Institute Research Council (IRC) approved project (Project ID: DSR 1.24/12).

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Correspondence to Shunmugiah Veluchamy Ramesh.

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Ramesh, S.V., Ratnaparkhe, M.B., Kumawat, G. et al. Plant miRNAome and antiviral resistance: a retrospective view and prospective challenges. Virus Genes 48, 1–14 (2014). https://doi.org/10.1007/s11262-014-1038-z

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