Advertisement

Plant Small RNAs: Big Players in Biotic Stress Responses

  • Mohini Prabha Singh
  • Pratiksha Singh
  • Rajesh Kumar Singh
  • R. Z. Sayyed
  • Anjney Sharma
Chapter
Part of the Microorganisms for Sustainability book series (MICRO, volume 13)

Abstract

A myriad of small RNAs (18–25 nt in length) undergo heterogeneous modifications to inflect RNA stability and other complex physiological processes like stress responses, metabolism, immunity, and epigenetic inheritance of environmentally acquired traits. Such small RNAs include microRNAs (miRNAs), PIWI-interacting RNAs (piRNAs), small interfering RNAs (siRNAs), and tRNA-derived small RNAs (tsRNAs). Worldwide crop production and human health are affected when plants are attacked by pathogens and pests. Therefore, a large collection of genes get up- or down regulated to mediate the defense responses in plants against pathogens (bacteria, fungi, oomycetes, and viruses). Host endogenous small RNAs, thus, come into play to counter biotic stress where RNA silencing machinery is utilized to facilitate pathogen-associated molecular pattern-triggered immunity and effector-triggered immunity. RNA interference (RNAi) pathways trigger gene silencing in interacting species from even different kingdoms (cross-kingdom RNAi). Diverse pathways are involved in regulating the defense mechanism including Dicer-like proteins (DCLs), double-stranded RNA (dsRNA) binding protein, RNA-dependent RNA polymerases (RDRs), RNA polymerase IV and V, small RNA methyltransferase HEN1, and Argonaute (AGO) proteins showcasing their functional specificities as well as verbosity. Transgenic plants are newly emerging players that help in solving the problem of pathogen attack in fields. In this chapter, the recent breakthrough on the function of sRNAs in response to biotic stress, mainly in plant-pathogen interaction, and its application in disease control is discussed.

Keywords

Biotic stress Small RNA Cross-kingdom RNAi Argonaute Gene silencing 

References

  1. Andika IB, Kondo H, Tamada T (2005) Evidence that RNA silencing-mediated resistance to beet necrotic yellow vein virus is less effective in roots than in leaves. Mol Plant-Microbe Interact 18:194–204PubMedCrossRefGoogle Scholar
  2. Axtell MJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64:137–159PubMedCrossRefGoogle Scholar
  3. Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P, Ilagan O, Johnson S, Plaetinck G, Munyikwa T, Pleau M, Vaughn T, Roberts J (2007) Control of coleopteran insect pests through RNA interference. Nat Biotechnol 25:1322–1326PubMedCrossRefGoogle Scholar
  4. Bonfim K, Faria JC, Nogueira EO, Mendes EA, Aragao FJ (2007) RNAi-mediated resistance to bean golden mosaic virus in genetically engineered common bean (Phaseolus vulgaris). Mol Plant-Microbe Interact 20:717–726.  https://doi.org/10.1094/MPMI-20-6-0717CrossRefPubMedGoogle Scholar
  5. Bebber DP, Gurr SJ (2015) Crop-destroying fungal and oomycete pathogens challenge food security. Fungal Genet Biol 74:62–64PubMedCrossRefGoogle Scholar
  6. Benkovics AH, Timmermans MC (2014) Developmental patterning by gradients of mobile small RNAs. Curr Opin Genet Dev 27:83–91PubMedCrossRefGoogle Scholar
  7. Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–366PubMedCrossRefGoogle Scholar
  8. Blevins T, Rajeswaran R, Shivaprasad PV, Beknazariants D, Si-Ammour A et al (2006) Four plant dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res 34:6233–6246PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bollman KM, Aukerman MJ, Park MY et al (2003) HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis. Development 130:1493–1504PubMedCrossRefGoogle Scholar
  10. Bond DM, Baulcombe DC (2014) Small RNAs and heritable epigenetic variation in plants. Trends Cell Biol 24:100–107PubMedCrossRefGoogle Scholar
  11. Boutet S, Vazquez F, Liu J, Beclin C, Fagard M et al (2003) Arabidopsis HEN1: a genetic link between endogenous miRNA controlling development and siRNA controlling transgene silencing and virus re-sistance. Curr Biol 13:843–848PubMedPubMedCentralCrossRefGoogle Scholar
  12. Campo S, Peris-Peris C, Sire C, Moreno AB, Donaire L, Zytnicki M et al (2013) Identification of a novel microRNA (miRNA) from rice that targets an alternatively spliced transcript of the Nramp6 (natural resistance-associated macrophage protein 6) gene involved in pathogen resistance. New Phytol 199:212–227PubMedCrossRefGoogle Scholar
  13. Chang SS, Zhang Z, Liu Y (2012) RNA interference pathways in fungi: mechanisms and functions. Annu Rev Microbiol 66:305–323PubMedPubMedCentralCrossRefGoogle Scholar
  14. Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8:884–896PubMedPubMedCentralCrossRefGoogle Scholar
  15. Chellappan P, Vanitharani R, Fauquet CM (2005) MicroRNA-binding viral protein interferes with Arabidopsis development. PNAS 102:10381–10386PubMedCrossRefGoogle Scholar
  16. Chen X (2005) MicroRNA biogenesis and function in plants. FEBS Lett 579:5923–5931PubMedPubMedCentralCrossRefGoogle Scholar
  17. Chen XM (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25:21–44PubMedPubMedCentralCrossRefGoogle Scholar
  18. 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 16:1302–1313PubMedPubMedCentralCrossRefGoogle Scholar
  19. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124(4):803–814PubMedCrossRefGoogle Scholar
  20. Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381PubMedCrossRefGoogle Scholar
  21. Cuellar WJ, Kreuze JF, Rajamaki ML, Cruzado KR, Untiveros M, Valkonen JP (2009) Elimination of antiviral defense by viral RNase III. Proc Natl Acad Sci U S A 106(25):10354–10358PubMedPubMedCentralCrossRefGoogle Scholar
  22. Cui X, Cao X (2014) Epigenetic regulation and functional exaptation of transposable elements in higher plants. Curr Opin Plant Biol 21:83–88PubMedCrossRefGoogle Scholar
  23. Curtin SJ, Watson JM, Smith NA, Eamens AL, Blanchard CL, Waterhouse PM (2008) The roles of plant dsRNA-binding proteins in RNAi-like pathways. FEBS Lett 582:2753–2760PubMedCrossRefGoogle Scholar
  24. Deleris A, Gallego-Bartolome J, Bao J, Kasschau KD, Carrington JC, Voinnet O (2006) Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313:68–71PubMedCrossRefGoogle Scholar
  25. Diaz-Pendon JA, Li F, Li WX, Ding SW (2007) 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(6):2053–2063PubMedPubMedCentralCrossRefGoogle Scholar
  26. Dickinson B, Zhang Y, Petrick JS, Heck G, Ivashuta S, Marshall WS (2013) Lack of detectable oral bioavailability of plant microRNAs after feeding in mice. Nat Biotechnol 31:965–967PubMedCrossRefGoogle Scholar
  27. Ding SW (2010) RNA-based antiviral immunity. Nat Rev Immuno 10:632–644CrossRefGoogle Scholar
  28. Dominissini D et al (2012) Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485:201–206PubMedPubMedCentralCrossRefGoogle Scholar
  29. Dominissini D et al (2016) The dynamic N1-methyladenosine methylome in eukaryotic messenger RNA. Nature 530:441–446PubMedPubMedCentralCrossRefGoogle Scholar
  30. Du P, Wu J, Zhang J, Zhao S, Zheng H, Gao G, Wei L, Li Y (2011) Viral infection induces expression of novel phased microRNAs from conserved cellular microRNA precursors. PLoS Pathog 7:e1002176PubMedPubMedCentralCrossRefGoogle Scholar
  31. Dunoyer P, Himber C, Voinnet O (2006) Induction, suppression and requirement of RNA silencing pathways in virulent Agrobacterium tumefaciens infections. Nat Genet 38(2):258–263PubMedCrossRefGoogle Scholar
  32. Ellendorff U, Fradin EF, de Jonge R, Thomma BP (2009) RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. J Exp Bot 60:591–602PubMedCrossRefGoogle Scholar
  33. Enrique R, Siciliano F, Favaro MA, Gerhardt N, Roeschlin R, Rigano L, Sendin L, Castagnaro A, Vojnov A, Marano MR (2011) Novel demonstration of RNAi in citrus reveals importance of citrus cal-lose synthase in defence against Xanthomonas citri subsp. citri. Plant Biotechnol J 9:394–407PubMedCrossRefGoogle Scholar
  34. Eschen-Lippold L, Landgraf R, Smolka U, Schulze S, Heilmann M, Heilmann I, Hause G, Rosahl S (2012) Activation of defense against Phytophthora infestans in potato by down-regulation of syntaxin gene expression. New Phytol 193:985–996PubMedCrossRefGoogle Scholar
  35. Escobar MA, Civerolo EL, Summerfelt KR, Dandekar AM (2001) RNAi-mediated oncogene silencing confers resistance to crown gall tumorigen-esis. Proc Natl Acad Sci U S A 98:13437–13442PubMedPubMedCentralCrossRefGoogle Scholar
  36. Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK et al (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16:939–944PubMedCrossRefGoogle Scholar
  37. 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(2):e219PubMedPubMedCentralCrossRefGoogle Scholar
  38. Feng F, Zhou JM (2012) Plant-bacterial pathogen interactions mediated by type III effectors. Curr Opin Plant Biol 15:469–476PubMedCrossRefGoogle Scholar
  39. 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 15:1494–1500PubMedCrossRefGoogle Scholar
  40. Goto K, Kobori T, Kosaka Y, Natsuaki T, Masuta C (2007) Characterization of silencing suppressor 2b of cucumber mosaic virus based on examination of its small RNA-binding abilities. Plant Cell Physiol 48(7):1050–1060PubMedCrossRefGoogle Scholar
  41. Haas G, Azevedo J, Moissiard G, Geldreich A, Himber C, Bureau M et al (2008) Nuclear import of CaMV P6 is required for infection and suppression of the RNA silencing factor DRB4. EMBO J 27:2102–2112PubMedPubMedCentralCrossRefGoogle Scholar
  42. Hammond SM, Bernstein E, Beach D, Hannon GJ (2000) An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404:293–296PubMedCrossRefGoogle Scholar
  43. Hannon GJ (2002) RNA interference. Nature 418(6894):244–251CrossRefGoogle Scholar
  44. He XF, Fang YY, Feng L, Guo HS (2008) Characterization of conserved and novel microRNAs and their targets, including a TuMV-induced TIR-NBS-LRR class R gene-derived novel miRNA in Brassica. FEBS Lett 582(16):2445–2452PubMedCrossRefGoogle Scholar
  45. Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N (2011) A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23:3812–3823PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hily JM, Ravelonandro M, Damsteegt V, Basset C, Petri C, Liu Z et al (2007) Plum pox virus coat protein gene intron-hair pin-RNA (ihpRNA) con-structs provide resistance to Plum pox virus in Nicotiana bethamiana and Prunus domestica. J Am Soc Hortic Sci 132:850–858CrossRefGoogle Scholar
  47. Hirschi KD (2012) New foods for thought. Trends Plant Sci 17:123–125PubMedCrossRefGoogle Scholar
  48. Huang G, Allen R, Davis EL, Baum TJ, Hussey RS (2006) Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proc Natl Acad Sci U S A 103:14302–14306PubMedPubMedCentralCrossRefGoogle Scholar
  49. Huckelhoven R (2007) Transport and secretion in plant-microbe interactions. Curr Opin Plant Biol 10:573–579PubMedCrossRefGoogle Scholar
  50. Hussain S et al (2013) Characterizing 5-methylcytosine in the mammalian epitranscriptome. Genome Biol 14:215PubMedPubMedCentralCrossRefGoogle Scholar
  51. Iwakawa H, Tomari Y (2013) Molecular insights into microRNA-mediated translational repression in plants. Mol Cell 52:591–601PubMedCrossRefGoogle Scholar
  52. Jagadeeswaran G, Saini A, Sunkar R (2009) Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 229:1009–1014PubMedCrossRefGoogle Scholar
  53. Jiang CJ, Shimono M, Maeda S, Inoue H, Mori M, Hasegawa M, Sugano S, Takatsuji H (2009) Suppression of the rice fatty-acid desaturase gene OsSSI2 enhances resistance to blast and leaf blight diseases in rice. Mol Plant Microbe Int 22:820–829CrossRefGoogle Scholar
  54. Jones JD, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329CrossRefGoogle Scholar
  55. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53CrossRefGoogle Scholar
  56. Kamachi S, Mochizuki A, Nishiguchi M, Tabei Y (2007) Transgenic Nicotiana benthamiana plants resistant to cucumber green mottlemosaic virus based on RNA silencing. Plant Cell Rep 26(1283):1288Google Scholar
  57. Kale SD, Tyler BM (2011) Entry of oomycete and fungal effectors into plant and animal host cells. Cell Microbiol 13:1839–1848PubMedCrossRefGoogle Scholar
  58. Katiyar-Agarwal S, Jin H (2010) Role of small RNAs in host-microbe interactions. Annu Rev Phytopathol 48:225–246PubMedPubMedCentralCrossRefGoogle Scholar
  59. 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 U S A 103:18002–18007PubMedPubMedCentralCrossRefGoogle Scholar
  60. Kawamata T, Tomari Y (2010) Making RISC. Trends Biochem Sci 35:368–376PubMedCrossRefGoogle Scholar
  61. Knip M, Constantin ME, Thordal-Christensen H (2014) Trans-kingdom cross-talk: small RNAs on the move. PLoS Genet 10:e1004602PubMedPubMedCentralCrossRefGoogle Scholar
  62. Koch A, Kogel KH (2014) New wind in the sails: improving the agronomic value of crop plants through RNAi-mediated gene silencing. Plant Biotechnol J 12:821–831PubMedCrossRefGoogle Scholar
  63. Koch A, Kumar N, Weber L, Keller H, Imani J, Kogel KH (2013) Host-induced gene silencing of cytochrome P450 lanosterol C14alpha-demethylase-encoding genes confers strong resistance to Fusarium species. Proc Natl Acad Sci U S A 110:19324–19329PubMedPubMedCentralCrossRefGoogle Scholar
  64. Krubphachaya P, Jurícek M, Kertbundit S (2007) Induction of RNA mediated resistance to papaya ring spot virus type. W J Biochem Mol Biol 40:401–411Google Scholar
  65. Lee RC, Feinbaum RL, Ambros V (1993) The C.elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854PubMedCrossRefPubMedCentralGoogle Scholar
  66. Li S, Mason CE (2014) The pivotal regulatory landscape of RNA modifications. Annu Rev Genomics Hum Genet 15:127–150PubMedCrossRefGoogle Scholar
  67. Li CF, Henderson IR, Song L, Fedoroff N, Lagrange T, Jacobsen SE (2008) Dynamic regulation of ARGONAUTE4 within multiple nuclear bodies in Arabidopsis thaliana. PLoS Genet 4:e27PubMedPubMedCentralCrossRefGoogle Scholar
  68. Li DH, Liu H, Yang Y, Zhen PP, Liang JS (2009) Down-regulated expression of RACK1 gene by RNA interference enhances drought tolerance in rice. Rice Sci 16:14–20CrossRefGoogle Scholar
  69. Li X, Zhu P, Ma S, Song J, Bai J, Sun F, Yi C (2015) Chemical pulldown reveals dynamic pseudouridylation of the mammalian transcriptome. Nat Chem Biol 11:592–597PubMedCrossRefPubMedCentralGoogle Scholar
  70. Liang G, Zhu Y, Sun B, Shao Y, Jing A, Wang J, Xiao Z (2014) Assessing the survival of exogenous plant microRNA in mice. Food Sci Nutr 2:380–388PubMedPubMedCentralCrossRefGoogle Scholar
  71. Mackey D, Holt BF, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108(6):743–754PubMedCrossRefGoogle Scholar
  72. Mao YB, Cai WJ, Wang JW, Hong GJ, Tao XY, Wang LJ, Huang YP, Chen XY (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat Biotechnol 25:1307–1313PubMedCrossRefGoogle Scholar
  73. Mayoral JG, Hussain M, Joubert DA, Iturbe-Ormaetxe I, O’Neill SL, Asgari S (2014) Wolbachia small noncoding RNAs and their role in cross-kingdom communications. Proc Natl Acad Sci U S A 111:18721–18726PubMedPubMedCentralCrossRefGoogle Scholar
  74. Missiou A, Kalantidis K, Boutla A, Tzortzakaki S, Tabler M, Tsagris M (2004) Generation of transgenic potato plants highly resistant to potato virus Y (PVY) through RNA silencing. Mol Breed 14:185–197CrossRefGoogle Scholar
  75. Mittelbrunn M, Sanchez-Madrid F (2012) Intercellular communication: diverse structures for exchange of genetic information. Nat Rev Mol Cell Biol 13:328–335PubMedPubMedCentralCrossRefGoogle Scholar
  76. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439PubMedCrossRefGoogle Scholar
  77. Navarro L, Jay F, Nomura K et al (2008) Suppression of the microRNA pathway by bacterial effector proteins. Science 321:964–967PubMedPubMedCentralCrossRefGoogle Scholar
  78. Niu QW, Lin SS, Reyes JL, Chen KC, Wu HW, Yeh SD et al (2006) Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat Biotechnol 24:1420–1428.  https://doi.org/10.1038/nbt1255CrossRefPubMedGoogle Scholar
  79. Pacheco R, Garcia-Marcos A, Barajas D, Martianez J, Tenllado F (2012) PVX-potyvirus synergistic infections differentially alter microRNA accumulation in Nicotiana benthamiana. Virus Res 165(2):231–235PubMedCrossRefGoogle Scholar
  80. Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495PubMedPubMedCentralCrossRefGoogle Scholar
  81. Park GG, Park JJ, Yoon J, Yu SN, An G (2010) A ring finger ligase gene, Oryza sativa delayed seed germination 1 (OsDSG1), controls seed germination and stress responses in rice. Plant Mol Bio 74:467–478CrossRefGoogle Scholar
  82. Pazhouhandeh M, Dieterle M, Marrocco K, Lechner E, Berry B et al (2006) F-box-like domain in the polerovirus protein P0 is required for silencing suppressor function. Proc Natl Acad Sci U S A 103:1994–1999PubMedPubMedCentralCrossRefGoogle Scholar
  83. Peltier AJ, Hatfield RD, Grau CR (2009) Soybean stem lignin concen expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol 6:3343–3353Google Scholar
  84. Pooggin M, Shivaprasad PV, Veluthambi K, Hohn T (2003) RNAi target-chalcone synthase gene into Petunia results in reversible cosuppression of ing of DNA virus in plants. Nat Biotechnol 21:131–132PubMedCrossRefGoogle Scholar
  85. Powell-Abel P, Nelson RS, De B, Hoffmann N, Rogers SG, Fraley RT (2006) A plant miRNA contributes to antibacterial resistance by repressing delay of disease development in transgenic plants that express the auxin signaling. Science 312:436–439CrossRefGoogle Scholar
  86. Qu F, Ye X, Hou G, Sato S, Clemente TE, Morris TJ (2005) RDR6 has a broad-spectrum but temperature-dependent antiviral defense role in Nicotiana benthamiana. J Virol 79:15209–15217PubMedPubMedCentralCrossRefGoogle Scholar
  87. Qu F, Ye X, Morris TJ (2008) Arabidopsis DRB4, AGO1, AGO7, and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. Proc Natl Acad Sci U S A 105:14732–14737PubMedPubMedCentralCrossRefGoogle Scholar
  88. Raja P, Sanville BC, Buchmann RC, Bisaro DM (2008) Viral genome methylation as an epigenetic defense against geminiviruses. J Virol 82:8997–9007PubMedPubMedCentralCrossRefGoogle Scholar
  89. Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R, Sun JY, Agrawal AA, Felton GW, Jander G (2012) Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol 158:854–863PubMedCrossRefGoogle Scholar
  90. Riechen J (2007) Establishment of broad-spectrum resistance against Blumeria germination and stress responses in rice MLO. J Verbrauch Lebensm 2:120CrossRefGoogle Scholar
  91. Robbins PD, Morelli AE (2014) Regulation of immune responses by extracellular vesicles. Nat Rev Immunol 14:195–208PubMedPubMedCentralCrossRefGoogle Scholar
  92. Rogers K, Chen X (2013) Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25:2383–2399PubMedPubMedCentralCrossRefGoogle Scholar
  93. Saleh MC, Tassetto M, van Rij RP, Goic B, Gausson V, Berry B, Jacquier C, Antoniewski C, Andino R (2009) Antiviral immunity in Drosophila requires systemic RNA interference spread. Nature 458:346–350PubMedPubMedCentralCrossRefGoogle Scholar
  94. Salido-Guadarrama I, Romero-Cordoba S, Peralta-Zaragoza O, Hidalgo-Miranda A, Rodriguez-Dorantes M (2014) MicroRNAs transported by exosomes in body fluids as mediators of intercellular communication in cancer. Onco Targets Ther 7:1327–1338PubMedPubMedCentralGoogle Scholar
  95. Saurabh S, Vidyarthi AS, Prasad D (2014) RNA interference: concept to reality in crop improvement. Planta 239:543–564PubMedCrossRefPubMedCentralGoogle Scholar
  96. Schauer SE, Jacobsen SE, Meinke DW, Ray A (2002) DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci 7:487–491PubMedCrossRefGoogle Scholar
  97. Seo JK, Wu J, Lii Y, Li Y, Jin H (2013) Contribution of small RNA pathway components in plant immunity. Mol Plant-Microbe Interact 26:617–625PubMedPubMedCentralCrossRefGoogle Scholar
  98. Shimizu T, Yoshii M, Wei T, Hirochika H, Omura T (2009) Silencing by RNAi of the gene for Pns12, a viroplasm matrix protein of Rice dwarf virus, results in strong resistance of transgenic rice plants to the virus. Plant Biotechnol J 7:24–32PubMedCrossRefGoogle Scholar
  99. Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos BA, Baulcombe DC (2012) A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24:859–874PubMedPubMedCentralCrossRefGoogle Scholar
  100. Simon-Mateo C, García JA (2011) Antiviral strategies in plants based on RNA silencing. Biochim Biophys Acta 1809:722–731.  https://doi.org/10.1016/j.bbagrm.2011.05.011CrossRefPubMedGoogle Scholar
  101. Trinks D, Rajeswaran R, Shivaprasad PV, Akbergenov R, Oakeley EJ et al (2005) Suppression of RNA silencing by a geminivirus nuclear protein, AC2, correlates with transactivation of host genes. J Virol 79:2517–2527PubMedPubMedCentralCrossRefGoogle Scholar
  102. Tsuda K, Katagiri F (2010) Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 3(4):459–465CrossRefGoogle Scholar
  103. Vaistij FE, Jones L, Baulcombe DC (2002) Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA-dependent RNA polymerase. Plant Cell 14:857–867PubMedPubMedCentralCrossRefGoogle Scholar
  104. 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(4):291–299PubMedPubMedCentralGoogle Scholar
  105. Vanderschuren H, Alder A, Zhang P, Gruissem W (2009) Dose-dependent RNAi-mediated geminivirus resistance in the tropical root crop cassava. Plant Mol Biol 70:265–272PubMedPubMedCentralCrossRefGoogle Scholar
  106. Vazquez F (2006) Arabidopsis endogenous small RNAs: highways and byways. Trends Plant Sci 11:460–468PubMedCrossRefGoogle Scholar
  107. Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687CrossRefGoogle Scholar
  108. Wang M, Abbott DC, Waterhouse PM (2000) A single copy of a virus-derived transgene encoding hairpin RNA gives immunity to barley yellow dwarf virus. Mol Plant Pathol 1:347–356PubMedCrossRefGoogle Scholar
  109. Wang H, Buckley KJ, Yang X, Buchmann RC, Bisaro DM (2005) Adenosine kinase inhibition and suppression of RNA silencing by geminivirus AL2 and L2 proteins. J Virol 79:7410–7418PubMedPubMedCentralCrossRefGoogle Scholar
  110. Wang Y, Li P, Cao X, Wang X, Zhang A, Li X (2009) Identification and expression analysis of miRNAs from nitrogen-fixing soybean nodules. Biochem Biophys Res Commun 378(4):799–803PubMedCrossRefGoogle Scholar
  111. Wang T, Chen L, Zhao M, Tian Q, Zhang WH (2011a) Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 12:367–378PubMedPubMedCentralCrossRefGoogle Scholar
  112. Wang XB, Jovel J, Udomporn P, Wang Y, Wu Q, Li WX, Gasciolli V, Vaucheret H, Ding SW (2011b) The 21-nucleotide, but not 22-nucleotide, viral secondary small interfering RNAs direct potent antiviral defense by two cooperative Argonautes in Arabidopsis thaliana. Plant Cell 23:1625–1638PubMedPubMedCentralCrossRefGoogle Scholar
  113. Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z, Kaloshian I, Huang HD, Jin H (2015) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118–123CrossRefGoogle Scholar
  114. Wu HW, Lin SS, Chen KC, Yeh SD, Chua NH (2010a) Discriminating mutations of HC-pro of zucchini yellow mosaic virus with differential effects on small RNA pathways involved in viral pathogenicity and symptom development. Mol Plant Microbe Interact 23(1):17–28PubMedCrossRefGoogle Scholar
  115. Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y (2010b) DNA methylation mediated by a microRNA pathway. Mol Cell 38:465–475PubMedCrossRefGoogle Scholar
  116. Xie Z, Fan B, Chen C, Chen Z (2001) An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense. Proc Natl Acad Sci U S A 98:6516–6521PubMedPubMedCentralCrossRefGoogle Scholar
  117. Xin M, Wang Y, Yao Y, Xie C, Peng H, Ni Z (2010) Diverse set of micro RNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biol 10:123–134.  https://doi.org/10.1186/1471-2229-10-123PubMedPubMedCentralCrossRefGoogle Scholar
  118. Yadav BC, Veluthambi K, Subramaniam K (2006) Host-generated double stranded RNA induces RNAi in plant-parasitic nematodes and protects the host from infection. Mol Biochem Parasitol 148:219–222PubMedCrossRefGoogle Scholar
  119. Yang L, Huang H (2014) Roles of small RNAs in plant disease resistance. J Integr Plant Biol 56:962–970PubMedCrossRefGoogle Scholar
  120. Yang Z, Ebright YW, Yu B et al (2006) HEN1 recognizes 21-24 nt small RNA duplexes and deposits a methyl group onto the 2′ OH of the 3′ terminal nucleotide. Nucleic Acids Res 34:667–675PubMedPubMedCentralCrossRefGoogle Scholar
  121. Yara A, Yaeno T, Hasegawa M, Seto H, Montillet JL, Kusumi K et al (2007) Disease resistance against Magnaporthe grisea is enhanced in transgenic rice with suppression of o-3 fatty acid desaturases. Plant Cell Physiol 48:1263–1274PubMedCrossRefGoogle Scholar
  122. Yin C, Park JJ, Gang DR, Hulbert SH (2014) Characterization of a tryptophan 2-monooxygenase gene from Puccinia graminis f. sp. tritici involved in auxin biosynthesis and rust pathogenicity. Mol Plant Microbe Interact 27:227–235PubMedCrossRefGoogle Scholar
  123. Yu D, Fan B, MacFarlane SA, Chen Z (2003) Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. Mol Plant-Microbe Interact 16:206–216PubMedCrossRefGoogle Scholar
  124. Zhang X, Zhao H, Gao S, Wang WC, Katiyar-Agarwal S, Huang HD, Raikhel N, Jin H (2011) Arabidopsis Argonaute 2 regulates innate immunity via miRNA393(∗)-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol Cell 42:356–366PubMedPubMedCentralCrossRefGoogle Scholar
  125. Zhuang JJ, Hunter CP (2012) RNA interference in Caenorhabditis elegans: uptake, mechanism, and regulation. Parasitology 139:560–573PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Mohini Prabha Singh
    • 1
  • Pratiksha Singh
    • 2
  • Rajesh Kumar Singh
    • 2
  • R. Z. Sayyed
    • 3
  • Anjney Sharma
    • 4
  1. 1.Department of Plant Breeding and GeneticsPunjab Agricultural UniversityLudhianaIndia
  2. 2.Agricultural College, State Key Laboratory of Subtropical Bioresources Conservation and UtilizationGuangxi UniversityNanningChina
  3. 3.Department of MicrobiologyPSGVP Mandal’s Arts, Science and Commerce CollegeShahadaIndia
  4. 4.ICAR-National Bureau of Agriculturally Important MicroorganismsMau Nath BhanjanIndia

Personalised recommendations