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RNAi for Resistance Against Biotic Stresses in Crop Plants

  • Pradeep Kumar Jain
  • Ramcharan Bhattacharya
  • Deshika Kohli
  • Raghavendra Aminedi
  • Pawan Kumar Agrawal
Chapter

Abstract

RNA interference (RNAi)-based gene silencing has become one of the most successful strategies in not only identifying gene function but also in improving agronomical traits of crops by silencing genes of different pathogens/pests and also plant genes for improvement of desired trait. The conserved nature of RNAi pathway across different organisms increases its applicability in various basic and applied fields. Here we attempt to summarize the knowledge generated on the fundamental mechanisms of RNAi over the years, with emphasis on insects and plant-parasitic nematodes (PPNs). This chapter also reviews the rich history of RNAi research, gene regulation by small RNAs across different organisms, and application potential of RNAi for generating transgenic plants resistant to major pests. But, there are some limitations too which restrict wider applications of this technology to its full potential. Further refinement of this technology in terms of resolving these shortcomings constitutes one of the thrust areas in present RNAi research. Nevertheless, its application especially in breeding agricultural crops resistant against biotic stresses will certainly offer the possible solutions for some of the breeding objectives which are otherwise unattainable.

Keywords

RNA interference RNAi Biotic stresses Insect resistance Disease resistance 

References

  1. Aalto AP, Pasquinelli AE (2012) Small non-coding RNAs mount a silent revolution in gene expression. Curr Opin Cell Biol 24:333–340PubMedPubMedCentralCrossRefGoogle Scholar
  2. Abdellatef E, Will T, Koch A et al (2015) Silencing the expression of the salivary sheath protein causes transgenerational feeding suppression in the aphid Sitobion avenae. Plant Biotechnol J B13:849–857CrossRefGoogle Scholar
  3. Agrawal N, Dasaradhi PVN, Mohmmed A et al (2003) RNA interference: biology, mechanism and applications. Microbiol Mol Biol Rev 67:657–685PubMedPubMedCentralCrossRefGoogle Scholar
  4. Ahringer J (ed) (2006) The C elegans research community. Reverse genetics J. http://www.wormbook.org
  5. Ajiro N, Miyamoto Y, Masunaka A et al (2010) Role of the host-selective ACT-toxin synthesis gene ACTTS2 encoding an enoylreductase in pathogenicity of the tangerine pathotype of Alternaria alternata. Phytopathology 100:120–126PubMedCrossRefPubMedCentralGoogle Scholar
  6. Allen ML, Walker WB (2012) Saliva of Lygus lineolaris digests double stranded ribonucleic acids. J Insect Physiol 58:391–396PubMedCrossRefPubMedCentralGoogle Scholar
  7. Alsford S, Turner DJ, Obado SO et al (2011) High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Res 21:915–924. https://doi.org/10.1101/gr.115089.110 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Anandalakshmi R, Pruss GJ, Ge X et al (1998) A viral suppressor of gene silencing in plants. Proc Natl Acad Sci U S A 95:13079–13084PubMedPubMedCentralCrossRefGoogle Scholar
  9. Andrade CE, Hunter WB (2016) RNA interference– natural gene-based technology for highly specific pest control (HiSPeC). In: Abdurakhmonov IY (ed) RNA interference. InTech, Croatia, pp 391–409Google Scholar
  10. Antonino JD, Coelho R, Lourenço T et al (2013) Knocking- down Meloidogyne incognita proteases by plant-delivered dsRNA has negative pleiotropic effect on nematode vigor. PLoS One 8:e85364. https://doi.org/10.1371/journal.pone.0085364 CrossRefGoogle Scholar
  11. Araujo RN, Santos A, Pinto FS et al (2006) RNA interference of the salivary gland nitrophorin 2 in the triatomine bug Rhodnius prolixus (Hemiptera: Reduviidae) by dsRNA ingestion or injection. Insect Biochem Mol Biol 36:683–693PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bai J, Sepp KJ, Perrimon N (2009) Culture of Drosophila primary cells dissociated from gastrula embryos and their use in RNAi screening. Nat Protoc 4:1502–1512PubMedCrossRefPubMedCentralGoogle Scholar
  13. Bakhetia M, Charlton W, Atkinson HJ et al (2005) RNA interference of dual oxidase in the plant nematode Meloidogyne incognita. Mol Plant Microbe Interact 18:1099–1106. https://doi.org/10.1094/MPMI-18-1099 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bakhetia M, Urwin PE, Atkinson HJ (2007) qPCR analysis and RNAi define pharyngeal gland cell-expressed genes of Heterodera glycines required for initial interactions with the host. Mol Plant Microbe Interact 20:306–312. https://doi.org/10.1094/mpmi-20-3-0306 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Banerjee S, Banerjee A, Gill SS et al (2017) RNA interference: a novel source of resistance to combat plant parasitic nematodes. Front Plant Sci 8:834. https://doi.org/10.3389/fpls.2017.00834 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Bansal R, Michel AP (2013) Core RNAi machinery and Sid1, a component for systemic RNAi, in the Hemipteran insect, Aphis glycines. Int J Mol Sci 14:3786–3801. https://doi.org/10.3390/ijms14023786 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Baum JA, Bogaert T, Clinton W et al (2007) Control of coleopteran insect pests through RNA interference. Nat Biotechnol 25:1322–1326. https://doi.org/10.1038/nbt1359 CrossRefPubMedGoogle Scholar
  18. Bautista MA, Miyata T, et a MK (2009) RNA interference-mediated knockdown of a cytochrome P450, CYP6BG1, from the diamondback moth, Plutella xylostella , reduces larval resistance to permethrin. Insect Biochem Mol Biol 39:38–46PubMedCrossRefPubMedCentralGoogle Scholar
  19. Berezikov E (2011) Evolution of microRNA diversity and regulation in animals. Nat Rev Genet 12(12):846–860PubMedCrossRefPubMedCentralGoogle Scholar
  20. Bernstein E, Caudy AA, Hammond SM et al (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–366PubMedCrossRefGoogle Scholar
  21. Bhatia V, Bhattacharya R, Uniyal PL et al (2012) Host generated siRNAs attenuate expression of serine protease gene in Myzus persicae. PLoS One 7(10):e46343. https://doi.org/10.1371/journal.pone.0046343 PubMedPubMedCentralCrossRefGoogle Scholar
  22. Bolognesi R, Ramaseshadri P, Anderson J et al (2012) Characterizing the mechanism of action of double-stranded RNA activity against western corn rootworm (Diabrotica virgifera virgifera LeConte). PLoSONE 7:e47534. https://doi.org/10.1371/journal.pone.0047534 CrossRefGoogle Scholar
  23. Bonning BC, Chougule NP (2014) Delivery of intrahemocoelic peptides for insect pest management. Trends Biotechnol 32:91–98PubMedCrossRefPubMedCentralGoogle Scholar
  24. Campbell ME, Budge GE, Bowman AS (2010) Gene-knockdown in the honey bee mite Varroa destructor by a non-invasive approach: studies on a glutathione S-transferase. Parasit Vectors 3:73. https://doi.org/10.1186/1756-3305-3-73 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Cappelle K, de Oliveira CFR, Eynde BV et al (2016) The involvement of clathrin-mediated endocytosis and two Sid-1-like transmembrane proteins in double-stranded RNA uptake in the Colorado potato beetle midgut. Insect Mol Biol 25:315–323PubMedCrossRefPubMedCentralGoogle Scholar
  26. Carmell MA, Xuan Z, Zhang MQ et al (2002) The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev 16:2733–2742PubMedCrossRefPubMedCentralGoogle Scholar
  27. Carneiro JS, Bastide PY, Chabot M et al (2010) Suppression of polygalacturonase gene expression in the phytopathogenic fungus Ophiostoma novo-ulmi by RNA interference. Fungal Genet Biol 47:399–405PubMedCrossRefPubMedCentralGoogle Scholar
  28. Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–655PubMedPubMedCentralCrossRefGoogle Scholar
  29. Caudy AA, Myers M, Hannon GJ et al (2002) Fragile X-related protein and VIG associate with RNA interference machinery. Genes Dev 16:2491–2496PubMedPubMedCentralCrossRefGoogle Scholar
  30. Chen Q, Rehman S, Smant G et al (2005) Functional analysis of pathogenicity proteins of the potato cyst nematode Globodera rostochiensis using RNAi. Mol. Plant Microb. Interact. 18:621–625CrossRefGoogle Scholar
  31. Chen J, Zhang D, Yao Q et al (2010) Feeding based RNA interference of a trehalose phosphate synthase gene in the brown plant hopper, Nilaparvata lugens. Insect Mol Biol 19:777–786PubMedCrossRefPubMedCentralGoogle Scholar
  32. Choudhary D, Koulagi R, Rohatagi D et al (2012) Engineering resistance against root-knot nematode, Meloidogyne incognita, by host delivered RNAi. In: Abstracts of international conference on plant biotechnology for food security: new frontiers. National Agricultural Science Centre, New Delhi, pp 21–24Google Scholar
  33. Christensen J, Litherland K, Faller T et al (2013) Metabolism studies of unformulated internally [3H]- labeled short interfering RNAs in mice. Drug Metab Dispos 41:1211–1219. https://doi.org/10.1124/dmd.112.050666 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Christiaens O, Sweveres L, Smagghe G (2014) DsRNA degradation in the pea aphid(Acyrthosiphon pisum) associated with lack of response in RNAi feeding and injection assay. Peptides 53:307–314PubMedCrossRefPubMedCentralGoogle Scholar
  35. Cogoni C, Macino G (2000) Post-transcriptional gene silencing across kingdoms. Curr Opin Genet Dev 10:638–643PubMedCrossRefPubMedCentralGoogle Scholar
  36. Coleman AD, Wouters RH, Mugford ST et al (2015) Persistence and transgenerational effect of plant-mediated RNAi in aphids. JExp Bot 66:541–548Google Scholar
  37. Coy MR, Sanscrainte ND, Chalaire KC et al (2012) Gene silencing in adult Aedes aegypti mosquitoes through oral delivery of double-stranded RNA. J Appl Entomol 136:741–748CrossRefGoogle Scholar
  38. Czauderna F, Fechtner M, Dames S et al (2003) Structural variations and stabilizing modifications of synthetic siRNAs in mammalian cells. Nucleic Acids Res 31:2705–2716. https://doi.org/10.1093/nar/gkg393 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Dalzell JJ, McVeigh P, Warnock et al (2011) RNAi effector diversity in nematodes. PLoS Negl Trop Dis 5:e1176PubMedPubMedCentralCrossRefGoogle Scholar
  40. Danchin EGJ, Arguel MJ, Campan-Fournier A et al (2013) Identification of novel target genes for safer and more specific control of root-knot nematodes from a pan-genome mining. PLoS Pathog 9:e1003745. https://doi.org/10.1371/journal.ppat.1003745 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Dang Y, Yang Q, Xue Z et al (2011) RNA interference in fungi: pathways, functions, and applications. Eukaryot Cell 10(9):1148–1155. https://doi.org/10.1128/EC.05109-11 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Daniel RGP, John AG (2008) RNAi-mediated crop protection against insects. Trends Biotechnol 26:393–400CrossRefGoogle Scholar
  43. Darrington M, Dalmay T, Morrison NI et al (2017) Implementing the sterile insect technique with RNA interference – a review. Entomol Exp Appl 164:155–175. https://doi.org/10.1111/eea.12575 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Deng F, Zhao Z (2014) Influence of catalase gene silencing on the survivability of Sitobion avenae. Arch Insect Biochem Physiol 86:46–57PubMedPubMedCentralGoogle Scholar
  45. Depicker A, Montagu MV (1997) Post-transcriptional gene silencing in plants. Curr Opin Cell Biol 9:373–382PubMedCrossRefPubMedCentralGoogle Scholar
  46. Dernburg AF, Karpen GH (2002) A chromosome RNAissance. Cell 111:159–162PubMedCrossRefPubMedCentralGoogle Scholar
  47. Dietzl G, Chen D, Schnorrer F et al (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448:151–156PubMedCrossRefPubMedCentralGoogle Scholar
  48. Dinh PTY, Brown CR, Elling AA (2014a) RNA interference of effector gene Mc16D10L confers resistance against Meloidogyne chitwoodi in Arabidopsis and Potato. Phytopathology 104:1098–1106. https://doi.org/10.1094/PHYTO-03-14-0063-R CrossRefPubMedPubMedCentralGoogle Scholar
  49. Dinh PTY, Zhang L, Brown CR et al (2014b) Plant mediated RNA interference of effector gene Mc16D10L confers resistance against Meloidogyne chitwoodi in diverse genetic backgrounds of potato and reduces pathogenicity of nematode offspring. Nematology 6:669–682. https://doi.org/10.1163/15685411-00002796 CrossRefGoogle Scholar
  50. Dorsett Y, Tuschl T (2004) siRNAs: applications in functional genomics and potential as therapeutics. Nat Rev Drug Discov 3:318–329. https://doi.org/10.1038/nrd1345 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Dowling D, Pauli T, Donath A et al (2016) Phylogenetic origin and diversification of RNAi pathway genes in insects. Genome Biol Evol 8:3784–3793. https://doi.org/10.1093/gbe/evw281 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Dutta TK, Papolu PK, Banakar P et al (2015) Tomato transgenic plants expressing hairpin construct of a nematode protease gene conferred enhanced resistance to root-knot nematodes. Front Microbiol 6:260. https://doi.org/10.3389/fmicb.2015.00260 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Dykxhoorn DM, Novina CD, Sharp PA (2003) Killing the messenger: short RNAs that silence gene expression. Nat Rev Mol Cell Biol 4:457–467PubMedCrossRefPubMedCentralGoogle Scholar
  54. Elbashir SM, Lendeckel W, Tuschl T (2001) RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev 15:188–200PubMedPubMedCentralCrossRefGoogle Scholar
  55. Fairbairn DJ, Cavallaro AS, Bernard M et al (2007) Host-delivered RNAi: an effective strategy to silence genes in plant parasitic nematodes. Planta 226:1525–1533. https://doi.org/10.1007/s00425-007-0588-x CrossRefPubMedPubMedCentralGoogle Scholar
  56. Fan W, Wei Z, Zhang M et al (2015a) Resistance to Ditylenchus destructor infection in sweet potato by the expression of small interfering RNAs targeting unc-15, a movement-related gene. Phytopahol 105:1458–1465. https://doi.org/10.1094/PHYTO-04-15-0087-R CrossRefGoogle Scholar
  57. Fan J, Zhang Y, Francis F et al (2015b) Orco mediates olfactory behaviors and winged morph differentiation induced by alarm pheromone in the grain aphid, Sitobion avenae. Insect Biochem Mol Biol 64:16–24PubMedCrossRefPubMedCentralGoogle Scholar
  58. Fanelli E, Di Vito M, Jones JT et al (2005) Analysis of chitin synthase function in a plant parasitic nematode, Meloidogyne artiellia, using RNAi. Gene 349:87–95PubMedCrossRefPubMedCentralGoogle Scholar
  59. Feinberg EH, Hunter CP (2003) Transport of dsRNA into cells by the transmembrane protein SID-1. Science 301:1545–1547PubMedCrossRefPubMedCentralGoogle Scholar
  60. Figueira-Mansur J, Ferreira-Pereira A, Mansur JF et al (2013) Silencing of P-glycoprotein increases mortality in temephos-treated Aedes aegypti larvae. Insect Biochem Mol Biol 22:648–658CrossRefGoogle Scholar
  61. Fire A, Xu S, Montgomery MK et al (1998) Potent and specific genetic interference by double-stranded RNA in C. elegans. Nature 391:806–811PubMedPubMedCentralCrossRefGoogle Scholar
  62. Garbian Y, Maori E, Kalev H et al (2012) Bidirectional transfer of RNAi between honey bee and Varroa destructor: Varroa gene silencing reduces Varroa population. PLoS Pathog 8(12):e1003035PubMedPubMedCentralCrossRefGoogle Scholar
  63. Gong L, Yang X, Zhang B et al (2011) Silencing of Rieske iron-sulfur protein using chemically synthesized siRNA as a potential biopesticide against Plutella xylostella. Pest Manag Sci 67:514–520PubMedCrossRefPubMedCentralGoogle Scholar
  64. Gong L, Chen Y, Hu Z et al (2013) Testing insecticidal activity of novel chemically synthesized sirna against Plutella xylostella under laboratory and field conditions. PLoSOne 8:e62990CrossRefGoogle Scholar
  65. Gong YH, Yu XR, Shang QL et al (2014) Oral delivery mediated RNA interference of a carboxylesterase gene results in reduced resistance to organophosphorus insecticides in the cotton aphid, Aphis gossypii glover. PLoS One 9:e102823PubMedPubMedCentralCrossRefGoogle Scholar
  66. Good L, Stach JEM (2011) Synthetic RNA silencing in bacteria antimicrobial discovery and resistance breaking. Front Microbiol 2:185PubMedPubMedCentralCrossRefGoogle Scholar
  67. Griebler M, Westerlund SA, Hoffmann KH et al (2008) RNA interference with the allato regulating neuropeptide genes from the fall armyworm Spodoptera frugiperda and its effects on the JH titer in the hemolymph. J Insect Physiol 54:997–1007PubMedCrossRefPubMedCentralGoogle Scholar
  68. Guo H, Song X, Wang G et al (2014) Plant-generated artificial small RNAs mediated aphid resistance. PLoS One 9:e97410PubMedPubMedCentralCrossRefGoogle Scholar
  69. Haegeman A, Joseph S, Gheysen G et al (2011) Analysis of the transcriptome of the root lesion nematode Pratylenchus coffeae generated by 454 sequencing technology. Mol Biochem Parasitol 178:7–14PubMedCrossRefPubMedCentralGoogle Scholar
  70. Hamann L, Jensen K, Harbers K (1993) Consecutive inactivation of both alleles of the gb110 gene has no effect on the proliferation and differentiation of mouse embryonic stem cells. Gene 126:279–284PubMedCrossRefPubMedCentralGoogle Scholar
  71. Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952PubMedPubMedCentralCrossRefGoogle Scholar
  72. Hammond SM, Caudy AA, Hannon GJ (2001) Post-transcriptional gene silencing by double-stranded RNA. Nat Rev Genet 2:110–119PubMedCrossRefPubMedCentralGoogle Scholar
  73. He B, Chu Y, Yin M et al (2013) Fluorescent nanoparticle delivered dsRNA toward genetic control of insect pests. Adv Mater Weinheim 25:4580–4584. https://doi.org/10.1002/adma.201301201 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Herrero-Vanrell R, Rincón AC, Alonso M et al (2005) Self-assembled particles of an elastin-like polymer as vehicles for controlled drug release. J Control Release 102:113–122. https://doi.org/10.1016/j.jconrel.2004.10.001 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Hernandez I, Chacon O, Rodriguez R et al. (2009) Black shank resistant tobacco by silencing of glutathione S- transferase. Biochem Biophys Res Commun 387:300–304PubMedCrossRefPubMedCentralGoogle Scholar
  76. Huang G, Allen R, Davis EL et al (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 103:14302–14306. https://doi.org/10.1073/pnas.0604698103 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Hull D, Timmons L (2004) Methods for delivery of double-stranded RNA into Caenorhabditis elegans. Methods Mol Biol 265:23–58PubMedPubMedCentralGoogle Scholar
  78. Huvenne H, Smagghe G (2010) Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J Insect Physiol 56:227–235. https://doi.org/10.1016/j.jinsphys.2009.10.004 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Ischizuka A, Siomi MC, Siomi H (2002) A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev 16:2497–2508CrossRefGoogle Scholar
  80. Jackson AL, Bartz SR, Schelter J et al (2003) Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol 21:635–637. https://doi.org/10.1038/nbt831 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Joga MR, Zotti MJ, Smagghe G et al (2016) RNAi efficiency, systemic properties, and novel delivery methods for pest insect control: what we know so far. Front Physiol 7:553. https://doi.org/10.3389/fphys.2016.00553 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Kamath RS, Martinez-Campos M, Zipperlen P et al (2001) Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol 2:2.1–2.10. https://doi.org/10.1186/gb-2000-2-1-research0002 CrossRefGoogle Scholar
  83. Kennerdell JR, Carthew RW (1998) Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2Act in the wingless pathway. Cell 95:1017–1026PubMedCrossRefPubMedCentralGoogle Scholar
  84. Ketting RF, Fischer SE, Bernstein E et al (2001) Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev 15:2654–2659PubMedPubMedCentralCrossRefGoogle Scholar
  85. Ketting RF (2011) The many faces of RNAi. Dev Cell 15:148-161. https://doi.org/10.1016/j.devcel.2011.01.012CrossRefGoogle Scholar
  86. Khajuria C, Buschman LL, Chen MS et al (2010) A gut-specific chitinase gene essential for regulation of chitin content of peritrophic matrix and growth of Ostrinia nubilalis larvae. Insect Biochem Mol Biol 40:621–629. https://doi.org/10.1016/j.ibmb.2010.06.003 CrossRefPubMedPubMedCentralGoogle Scholar
  87. Klink VP, Kim KH, Martins V et al (2009) A correlation between host-mediated expression of parasite genes as tandem inverted repeats and abrogation of development of female Heterodera glycines cyst formation during infection of Glycine max. Planta 230:53–71. https://doi.org/10.1007/s00425-009-0926-2 CrossRefPubMedPubMedCentralGoogle Scholar
  88. 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 12:821–831PubMedCrossRefPubMedCentralGoogle Scholar
  89. Koch A, Kumar N, Weber L et al (2013) Host-induced gene silencing of cytochrome P450 lanosterol C14α-demethylase-encoding genes confers strong resistance to Fusarium species. Proc Natl Acad Sci U S A 110(48):19324–19329. pmid:24218613PubMedPubMedCentralCrossRefGoogle Scholar
  90. Kontogiannatos D, Swevers L, Maenaka K et al (2013) Functional characterization of a juvenile hormone esterase related gene in the moth Sesamia nonagrioides through RNA interference. PLoS One 8:e73834PubMedPubMedCentralCrossRefGoogle Scholar
  91. Kumar M, Gupta GP, Rajam MV (2009) Silencing of acetyl cholinesterase gene of Helicoverpa armigera by siRNA affects larval growth and its life cycle. J Insect Physiol 55:273–278. https://doi.org/10.1016/j.jinsphys.2008.12.005 CrossRefPubMedPubMedCentralGoogle Scholar
  92. Kumar A, Wang S, Ou R et al (2013) Development of an RNAi based microalgal larvicide to control mosquitoes. Malaria World J 4:6Google Scholar
  93. Kumar A, Kakrana A, Sirohi A et al (2017) Host-delivered RNAi-mediated root-knot nematode resistance in Arabidopsis by targeting splicing factor and integrase genes. J Gen Plant Pathol 83:91–97. https://doi.org/10.1007/s10327-017-0701-3 CrossRefGoogle Scholar
  94. Kurreck J (2003) Antisense technologies: improvement through novel chemical modifications. Eur J Biochem 270:1628–1644. https://doi.org/10.1046/j.1432-1033.2003.03555.x CrossRefPubMedPubMedCentralGoogle Scholar
  95. Kwon DH, Park JH, Lee SH (2013) Screening of lethal genes for feeding RNAi by leaf disc-mediated systematic delivery of dsRNA in Tetranychus urticae. Pestic Biochem Physiol 105:69–75. https://doi.org/10.1016/j.pestbp.2012.12.001 PubMedCrossRefPubMedCentralGoogle Scholar
  96. Lacroix H, Spanu PD (2009) Silencing of six hydrophobins in Cladosporium fulvum: complexities of simultaneously targeting multiple genes. Appl Environ Microbiol 75:542–546PubMedCrossRefPubMedCentralGoogle Scholar
  97. Lendner M, Doligalska M, Lucius R et al. (2008) Attempts to establish RNA interference in the parasitic nematode Heligmosomoides polygyrus. Mol Biochem Parasitol 161:21–31PubMedCrossRefPubMedCentralGoogle Scholar
  98. Li J, Todd TC, Oakley TR et al (2010a) Host-derived suppression of nematode reproductive and fitness genes decreases fecundity of Heterodera glycines Ichinohe. Planta 232:775–785. https://doi.org/10.1007/s00425-010-1209-7 CrossRefPubMedPubMedCentralGoogle Scholar
  99. Li J, Todd TC, Trick HN (2010b) Rapid in planta evaluation of root expressed transgenes in chimeric soybean plants. Plant Cell Rep 29:113–123. https://doi.org/10.1007/s00299-009-0803-2 CrossRefPubMedPubMedCentralGoogle Scholar
  100. Li J, Chen Q, Lin Y et al (2011a) RNA interference in Nilaparvata lugens (Homoptera, Delphacidae) based on dsRNA ingestion. Pest Manag Sci 67:852–859PubMedCrossRefPubMedCentralGoogle Scholar
  101. Li X, Zhang M, Zhang H (2011b) RNA interference of four genes in adult Bactrocera dorsalis by feeding their dsRNAs. PLoS One 6:e17788PubMedPubMedCentralCrossRefGoogle Scholar
  102. Li J, Todd TC, Lee J et al (2011c) Biotechnological application of functional genomics towards plant parasitic nematode control. Plant Biotech J 9:936–944. https://doi.org/10.1111/j.1467–7652.2011.00601.x CrossRefGoogle Scholar
  103. Li J, Wang XP, Wang MQ et al (2013) Advances in the use of the RNA interference technique in Hemiptera. Insect Sci 20:31–39. https://doi.org/10.1111/j.1744-7917.2012.01550.x CrossRefPubMedPubMedCentralGoogle Scholar
  104. Li XQ, Wei JZ, Tan A et al. (2007) Resistance to root-knot nematode in tomato roots expressing a nematicidal Bacillus thuringiensis crystal protein. Plant Biotechnol J 5:455-464. https://doi.org/10.1111/j.1467-7652.2007.00257.x PubMedCrossRefPubMedCentralGoogle Scholar
  105. Li Y, Wang K, Xie H et al (2015) Cathepsin B cysteine proteinase is essential for the development and pathogenesis of the plant parasitic nematode Radopholus similis. Int J Biol Sci 11:1073–1087. https://doi.org/10.7150/ijbs.12065 CrossRefPubMedPubMedCentralGoogle Scholar
  106. Lilley CJ, Goodchild SA, Atkinson HJ et al (2005) Cloning and characterisation of a Heterodera glycines aminopeptidase cDNA. Int J Parasitol 35:1577–1585PubMedCrossRefPubMedCentralGoogle Scholar
  107. Lim LP, Glasner ME, Yekta S et al (2003) Vertebrate micro-RNA genes. Science 299:1540PubMedCrossRefPubMedCentralGoogle Scholar
  108. Lindbo JA, Silva-Rosales L, Proebsting WM et al (1993) Induction of a highly specific antiviral state in transgenic plants: implications for regulation of gene expression and virus resistance. Plant Cell 5:1749–1759PubMedPubMedCentralCrossRefGoogle Scholar
  109. Lipardi C, Wei Q, Paterrson BM (2001) RNAi as random degradation PCR: siRNA primers convert mRNA into dsRNA that are degraded to generate new siRNAs. Cell 101:297–307CrossRefGoogle Scholar
  110. Lorenz C, Hadwiger P, John M et al (2004) Steroid and lipid conjugates of siRNAs to enhance cellular uptake and gene silencing in liver cells. Bioorg Med Chem Lett 14:4975–4977. https://doi.org/10.1016/j.bmcl.2004.07.018 CrossRefPubMedPubMedCentralGoogle Scholar
  111. Lourenço-Tessutti IT, Souza JDA, Martins-de-Sa D et al (2015) Knockdown of heat-shock protein 90 and isocitrate lyase gene expression reduced root-knot nematode reproduction. Phytopathology 105:628–637. https://doi.org/10.1094/PHYTO-09-14-0237-R CrossRefPubMedPubMedCentralGoogle Scholar
  112. Lum L, Yao S, Mozer B et al (2003) Identification of Hedgehog pathway components by RNAi in Drosophila cultured cells. Science 299:2039–2045PubMedCrossRefPubMedCentralGoogle Scholar
  113. Luo Y, Wang X, Wang X et al (2013) Differential responses of migratory locusts to systemic RNA interference via double-stranded RNA injection and feeding. Insect Mol Biol 22:574–583. https://doi.org/10.1111/imb.12046 CrossRefPubMedPubMedCentralGoogle Scholar
  114. Macrae IJ, Zhou K, Li F et al (2006) Structural basis for double-stranded RNA processing by Dicer. Science 311:195–198PubMedCrossRefPubMedCentralGoogle Scholar
  115. Majumdar R, Rajasekaran K, Cary JW (2017) RNA interference (RNAi) as a potential tool for control of mycotoxin contamination in crop plants: concepts and considerations. Front Plant Sci 8:200. https://doi.org/10.3389/fpls.2017.00200 CrossRefPubMedPubMedCentralGoogle Scholar
  116. Manoharan M (2003) RNA interference and chemically modified siRNAs. Nucleic Acids Res Suppl 3:115–116. https://doi.org/10.1093/nass/3.1.115 CrossRefGoogle Scholar
  117. Mao J, Zeng F (2012) Feeding-based RNA interference of a gap gene is lethal to the pea aphid, Acyrthosiphon pisum. PLoS One 7:e48718PubMedPubMedCentralCrossRefGoogle Scholar
  118. Mao J, Zeng F (2014) Plant-mediated RNAi of a gap gene-enhanced tobacco tolerance against the Myzus persicae. Transgenic Res 23:145–152. https://doi.org/10.1007/s11248-013-9739-y CrossRefPubMedPubMedCentralGoogle Scholar
  119. Mao YB, Cai WJ, Wang JW et al (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat Biotechnol 25:1307–1313. https://doi.org/10.1038/nbt1352 CrossRefPubMedGoogle Scholar
  120. Mao YB, Tao XY, Xue XY et al (2011) Cotton plants expressing CYP6AE14 double-stranded RNA show enhanced resistance to bollworms. Transgenic Res 20:665–673. https://doi.org/10.1007/s11248-010-9450-1 CrossRefPubMedPubMedCentralGoogle Scholar
  121. Mao YB, Xue XY, Tao XY et al (2013) Cysteine protease enhances plant-mediated bollworm RNA interference. Plant Mol Biol 83:119–129. https://doi.org/10.1007/s11103-013-0030-7 CrossRefPubMedPubMedCentralGoogle Scholar
  122. Matzke M, Matzke AJ, Kooter JM (2001) RNA: guiding gene silencing. Science 293:1080–1083PubMedCrossRefPubMedCentralGoogle Scholar
  123. Maule AG, McVeigh P, Dalzell JJ et al (2011) An eye on RNAi in nematode parasites. Trends Parasitol 27:505–513. https://doi.org/10.1016/j.pt.2011.07.004 CrossRefPubMedPubMedCentralGoogle Scholar
  124. McDonald T, Brown D, Keller NP et al (2005) RNA silencing of mycotoxin production in Aspergillus and Fusarium species. Mol Plant-Microbe Interact 18:539–545PubMedCrossRefPubMedCentralGoogle Scholar
  125. McEwan DL, Weisman AS, Hunter CP (2012) Uptake of extracellular double-stranded RNA by SID-2. Mol Cell 47:746–754. https://doi.org/10.1016/j.molcel.2012.07.014 CrossRefPubMedPubMedCentralGoogle Scholar
  126. Meer VRK, Choi MY (2013) Formicidae (ant) control using double-stranded RNA constructs. US Patent No. 8,575,328Google Scholar
  127. Meyering-Vos M, Muller A (2007) RNA interference suggests sulfakinins as satiety effectors in the cricket Gryllus bimaculatus. J Insect Physiol 53:840–848PubMedCrossRefPubMedCentralGoogle Scholar
  128. Miller SC, Miyata K, Brown SJ et al (2012) Dissecting systemic RNA interference in the red flour beetle Tribolium castaneum: parameters affecting the efficiency of RNAi. PLoS One 7:e47431. https://doi.org/10.1371/journal.pone.0047431 CrossRefPubMedPubMedCentralGoogle Scholar
  129. Mitter N, Worrall EA, Robinson KE et al (2017) Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nature Plants 3:16207PubMedCrossRefPubMedCentralGoogle Scholar
  130. Miyamoto Y, Masunaka A, Tsuge T et al (2008) Functional analysis of a multicopy host-selective ACT-toxin biosynthesis gene in the tangerine pathotype of Alternaria alternata using RNA silencing. Mol Plant-Microbe Interact 21:1591–1599PubMedCrossRefPubMedCentralGoogle Scholar
  131. Mutti NS, Park Y, Reese JC et al (2006) RNAi knockdown of a salivary transcript leading to lethality in the pea aphid, Acyrthosiphon pisum. J Insect Sci 6:38PubMedCentralCrossRefGoogle Scholar
  132. Naessens E, Dubreuil G, Giordanengo P et al (2015) A secreted MIF cytokine enables aphid feeding and represses plant immune responses. Curr Biol 25:1898–1903PubMedCrossRefPubMedCentralGoogle Scholar
  133. Nakai K, Horton P (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24:34–36PubMedCrossRefPubMedCentralGoogle Scholar
  134. Napoli C, Lemieux C, Jorgensen R (1990) Introduction of a chimeric chalcone synthase gene into Petunia results in reversible cosuppression of homologous genes in trans. Plant Cell 2:279–289PubMedPubMedCentralCrossRefGoogle Scholar
  135. Niu JH, Jian H, Xu J et al (2012) RNAi silencing of the Meloidogyne incognita Rpn7 gene reduces nematode parasitic success. Euro J Plant Pathol 134:131–144. https://doi.org/10.1007/s10658-012-9971-y CrossRefGoogle Scholar
  136. Niu J, Liu P, Liu Q et al (2016) Msp40 effector of root-knot nematode manipulates plant immunity to facilitate parasitism. Sci Rep 6:19443. https://doi.org/10.1038/srep19443 CrossRefPubMedPubMedCentralGoogle Scholar
  137. Nowara D, Gay A, Lacomme C et al (2010) HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 22:3130–3141. https://doi.org/10.1105/tpc.110.077040 CrossRefPubMedPubMedCentralGoogle Scholar
  138. Nunes CC, Dean RA (2012) Host-induced gene silencing: a tool for understanding fungal host interaction and for developing novel disease control strategies. Mol Plant Pathol 13:519–529. https://doi.org/10.1111/J.1364-3703.2011.00766.X CrossRefPubMedGoogle Scholar
  139. Nunes FMF, Simoes ZLP (2009) A non-invasive method for silencing gene transcription in honeybees maintained under natural conditions. Insect Biochem Mol Biol 39:157–160PubMedCrossRefPubMedCentralGoogle Scholar
  140. Nykanen A, Haley B, Zamore PD (2001) ATP requirement and small interfering RNA structure in the RNA interference pathway. Cell 107:309–321PubMedCrossRefPubMedCentralGoogle Scholar
  141. Ober KA, Jockusch EL (2006) The roles of wingless and decapentaplegic in axis and appendage development in the red flour beetle, Tribolium castaneum. Dev Biol 294:391–405PubMedCrossRefPubMedCentralGoogle Scholar
  142. Panwar V, McCallum B, Bakkeren G (2013) Host-induced gene silencing of wheat leaf rust fungus Puccinia triticina pathogenicity genes mediated by the Barley stripe mosaic virus. Plant Mol Biol 81:595–608. https://doi.org/10.1007/s11103-013-0022-7 CrossRefPubMedPubMedCentralGoogle Scholar
  143. Papolu PK, Gantasala NP, Kamaraju D et al (2013) Utility of host delivered RNAi of two FMRF amide like peptides, flp-14 and flp-18, for the management of root knot nematode, Meloidogyne incognita. PLoS One 8:e80603. https://doi.org/10.1371/journal.pone.0080603 CrossRefPubMedPubMedCentralGoogle Scholar
  144. Pasquinelli AE (2002) MicroRNAs: deviants no longer. Trends Genet 18:171–173PubMedCrossRefPubMedCentralGoogle Scholar
  145. Peng T, Pan Y, Yang C et al (2016) Over-expression of CYP6A2 is associated with spirotetramat resistance and cross-resistance in the resistant strain of Aphis gossypii glover. Pestic Biochem Physiol 126:64–69PubMedCrossRefPubMedCentralGoogle Scholar
  146. Pitino M, Hogenhout SA (2013) Aphid protein effectors promote aphid colonization in a plant species-specific manner. Mol Plant-Microbe Interact 26:130–139PubMedCrossRefPubMedCentralGoogle Scholar
  147. Pitino M, Coleman AD, Maffei ME et al (2011) Silencing of aphid genes by dsRNA feeding from plants. PLoSONE 6:e25709. https://doi.org/10.1371/journal.pone.0025709 CrossRefGoogle Scholar
  148. Possamai SJ, Trionnaire GL, Bonhomme J et al (2007) Gene knockdown by RNAi in the pea aphid Acyrthosiphon pisum. BMC Biotechnol 7:63CrossRefGoogle Scholar
  149. Price DR, Gatehouse JA (2008) RNAi-mediated crop protection against insects. Trends Biotechnol 26:393–400. https://doi.org/10.1016/j.tibtech.2008.04.004 CrossRefPubMedPubMedCentralGoogle Scholar
  150. Rajagopal R, Sivakumar S, Agrawal N et al (2002) Silencing of midgut aminopeptidase N of Spodoptera litura by double-stranded RNA establishes its role as Bacillus thuringiensis toxin receptor. J Biol Chem 277:46849–46851PubMedCrossRefPubMedCentralGoogle Scholar
  151. Rangasamy M, Siegfried BD (2012) Validation of RNA interference in western corn rootworm Diabrotica virgifera virgifera LeConte (Coleoptera, Chrysomelidae) adults. Pest Manag Sci 68:587–591. https://doi.org/10.1002/ps.2301 CrossRefPubMedPubMedCentralGoogle Scholar
  152. Rebijith KB, Asokan R, Hande HR et al (2016) RNA interference of odorant-binding protein 2 (OBP2) of the cotton aphid, Aphis gossypii (glover), resulted in altered electrophysiological responses. Appl Biochem Biotechnol 178:251–266PubMedCrossRefPubMedCentralGoogle Scholar
  153. Riechen J (2007) Establishment of broad-spectrum resistance against Blumeria graminis f. sp. tritici in Triticum aestivum by RNAi-mediated knock-down of MLO. J Verbrauch Lebensm 2:120. https://doi.org/10.1007/s00003-007-0282-8 CrossRefGoogle Scholar
  154. Rodriguez-Cabrera L, Trujillo-Bacallao D, Borra’s-Hidalgo O et al (2010) RNAi-mediated knockdown of a Spodoptera frugiperda trypsin-like serine-protease gene reduces susceptibility to a Bacillus thuringiensis Cry1Ca1 protoxin. Environ Microbiol 12:2894–2903PubMedCrossRefPubMedCentralGoogle Scholar
  155. Romano N, Macino G (1992) Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol 6:3343–3353PubMedPubMedCentralCrossRefGoogle Scholar
  156. Rosso MN, Dubrana MP, Cimbolini N et al (2005) Application of RNA interference to root-knot nematode genes encoding esophageal gland proteins. Mol. Plant Microb. Interact. 18:615–620. https://doi.org/10.1094/MPMI-18-0615 CrossRefGoogle Scholar
  157. Roxström-Lindquist K, Terenius O, Faye I (2004) Parasite-specific immune response in adult Drosophila melanogaster: a genomic study. Scientific Report 5:207–212. https://doi.org/10.1038/sj.embor.7400073 CrossRefGoogle Scholar
  158. Santos AC, Sena JAL, Santos SC et al (2009) dsRNA induced gene silencing in Moniliophthora perniciosa, the causal agent of witches’ broom disease of cacao. Fungal Genet Biol 46:825–836PubMedCrossRefGoogle Scholar
  159. Sapountzis P, Duport G, Balmand S et al (2014) New insight into the RNA interference response against cathepsin-L gene in the pea aphid, Acyrthosiphon pisum: molting or gut phenotypes specifically induced by injection or feeding treatments. Insect Biochem Mol Biol 51:20–32PubMedCrossRefPubMedCentralGoogle Scholar
  160. Schmidt A, Palumbo G, Bozzetti MP et al (1999) Genetic and molecular characterization of sting, a gene involved in crystal formation and meiotic drive in the male germ line of Drosophila melanogaster. Genetics 151:749–760PubMedPubMedCentralGoogle Scholar
  161. Senthil-Kumar M, Mysore KS (2011) Caveat of RNAi in plants: the off-target effect. In: Kodama H, Komamine A (eds) RNAi and plant gene function analysis. Methods in molecular biology (methods and protocols), vol 744. Humana PressGoogle Scholar
  162. Shakesby AJ, Wallace IS, Isaacs HV et al (2009) A water-specific aquaporin involved in aphid osmoregulation. Insect Biochem Mol Biol 39:1–10. https://doi.org/10.1016/j.ibmb.2008.08.008 CrossRefPubMedGoogle Scholar
  163. Shivakumara TN, Sonam C, Divya K et al (2017) Host-induced silencing of two pharyngeal gland genes conferred transcriptional alteration of cell wall-modifying enzymes of Meloidogyne incognita vis-à-vis perturbed nematode infectivity in eggplant. Front Plant Sci 8:473. https://doi.org/10.3389/fpls.2017.00473 CrossRefPubMedPubMedCentralGoogle Scholar
  164. Sijen T, Fleenor J, Simmer F et al (2001) On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107:465–476PubMedPubMedCentralCrossRefGoogle Scholar
  165. Sindhu A, Maier TR, Mittchum MG et al (2009) Effective and specific in planta RNAi in cyst nematodes: expression interference of four parasitism genes reduces parasitic success. J Exp Bot 1:315–324. https://doi.org/10.1093/jxb/ern289 CrossRefGoogle Scholar
  166. Singh AD, Wong S, Ryan CP et al (2013) Oral delivery of double-stranded RNA in larvae of the yellow fever mosquito, Aedes aegypti: implications for pest mosquito control. J Insect Sci 13:69PubMedPubMedCentralCrossRefGoogle Scholar
  167. Siomi H, Siomi MC (2009) On the road to reading the RNA-interference code. Nature 457:396–404. https://doi.org/10.1038/nature07754 CrossRefPubMedPubMedCentralGoogle Scholar
  168. Steeves RM, Todd TC, Essig JS et al (2006) Transgenic soybeans expressing siRNAs specific to a major sperm protein gene suppress Heterodera glycines reproduction. Func Plant Biol 33:991–999. https://doi.org/10.1071/FP06130 CrossRefGoogle Scholar
  169. Surakasi VP, Mohamed AAM, Kim Y (2011) RNA interference of β1 integrin subunit impairs development and immune responses of the beet armyworm, Spodoptera exigua. J Insect Physiol 57:1537–1544PubMedCrossRefPubMedCentralGoogle Scholar
  170. Tabara H, Grishok A, Mello CC (1998) RNAi in C. elegans: soaking in the genome sequence. Science 282:430–431. https://doi.org/10.1126/science.282.5388.430 CrossRefPubMedPubMedCentralGoogle Scholar
  171. Tabashnik BE (2008) Delaying insect resistance to transgenic crops. PNAS 105:19029–19030. https://doi.org/10.1073/pnas.0810763106 PubMedCrossRefPubMedCentralGoogle Scholar
  172. Tabashnik BE, Gassmann AJ, Crowder DW et al (2008) Insect resistance to Bt crops: evidence versus theory. Nat Biotechnol 26:199–202. https://doi.org/10.1038/nbt1382 CrossRefPubMedPubMedCentralGoogle Scholar
  173. Tan FL, Yin JQ (2004) RNAi, a new therapeutic strategy against viral infection. Cell Res 14:460–466PubMedCrossRefPubMedCentralGoogle Scholar
  174. Terenius O, Papanicolaou A, Garbutt JS et al (2011) RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J Insect Physiol 57:231–245. https://doi.org/10.1016/j.jinsphys.2010.11.006 CrossRefPubMedPubMedCentralGoogle Scholar
  175. Thompson JD, Kornbrust DJ, Foy JW et al (2012) Toxicological and pharmacokinetic properties of chemically modified siRNAs targeting p53 RNA following intravenous administration. Nucleic Acid Ther 22:255–264. https://doi.org/10.1089/nat.2012.0371 CrossRefPubMedPubMedCentralGoogle Scholar
  176. Tian H, Peng H, Yao Q et al (2009) Developmental control of a lepidopteran pest Spodoptera exigua by ingestion of bacteria expressing dsRNA of a non-midgut gene. PLoS One 4:e6225PubMedPubMedCentralCrossRefGoogle Scholar
  177. Timmons L, Court DL, Fire A (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263:103–112. https://doi.org/10.1016/S0378-1119(00)00579-5 CrossRefPubMedPubMedCentralGoogle Scholar
  178. Tinoco ML, Dias BB, Astta RCD et al (2010) In vivo trans-specific gene silencing in fungal cells by in planta expression of a double-stranded RNA. BMC Biol 8:1–11CrossRefGoogle Scholar
  179. Tomari Y, Zamore PD (2005) MicroRNA biogenesis: drosha can't cut it without a partner. Curr Biol 15:R61–R64PubMedCrossRefPubMedCentralGoogle Scholar
  180. Tomoyasu Y, Miller SC, Tomita S et al (2008) Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biol 9:R10. https://doi.org/10.1186/gb-2008-9-1-r10 CrossRefPubMedPubMedCentralGoogle Scholar
  181. Turner CT, Davy MW, MacDiarmid RM et al (2006) RNA interference in the light brown apple moth, Epiphyas postvittana Walker induced by double-stranded RNA feeding. Insect Mol Biol 15:383–391PubMedCrossRefPubMedCentralGoogle Scholar
  182. Tuschl T, Zamore PD, Lehmann R et al (1999) Targeted mRNA degradation by double-stranded RNA in vitro. Genes Dev 13:3191–3197PubMedPubMedCentralCrossRefGoogle Scholar
  183. Tzin V, Yang X, Jing X et al (2015) RNA interference against gut osmoregulatory genes in phloem-feeding insects. J Insect Physiol 79:105–112PubMedCrossRefPubMedCentralGoogle Scholar
  184. Ulvila J, Parikka M, Kleino A et al (2006) Double-stranded RNA is internalized by scavenger receptor-mediated endocytosis in Drosophila S2 cells. J Biol Chem 281:14370–14375PubMedCrossRefPubMedCentralGoogle Scholar
  185. Upadhyay SK, Chandrashekar K, Thakur N et al (2011) RNA interference for the control of whiteflies (Bemisia tabaci) by oral route. J Biosci 36:153–161PubMedCrossRefPubMedCentralGoogle Scholar
  186. Urwin PE, Lilley CJ, Atkinson HJ (2002) Ingestion of double-stranded RNA by pre-parasitic juvenile cyst nematodes leads to RNA interference. Mol Plant Microb Interact 15:747–752. https://doi.org/10.1094/MPMI.2002.15.8.747 CrossRefGoogle Scholar
  187. Urwin PE, Lilley CJ, McPherson MJ et al. (1997) Resistance to both cyst‐ and root‐knot nematodes conferred by transgenic Arabidopsis expressing a modified plant cystatin. Plant J 12:455–461PubMedCrossRefPubMedCentralGoogle Scholar
  188. Valdes VJ, Sampieri A, Sepulveda J et al (2003) With double stranded RNA to prevent in vitro and in vivo viral infections by recombinant baculovirus. J Biol Chem 278:19317–19324PubMedCrossRefPubMedCentralGoogle Scholar
  189. Van Rij RP, Berezikov E (2009) Small RNAs and the control of transposons and viruses in Drosophila. Trends Microbiol 17:163–171PubMedCrossRefPubMedCentralGoogle Scholar
  190. Vauthier C, Dubernet C, Chauvierre C et al (2003) Drug delivery to resistant tumors: the potential of poly (alkyl cyanoacrylate) nanoparticles. J Control Release 93:151–160. https://doi.org/10.1016/j.jconrel.2003.08.005 CrossRefPubMedPubMedCentralGoogle Scholar
  191. Vieira P, Akker EDS, Verma R et al (2015) The Pratylenchus penetrans transcriptome as a source for the development of alternative control strategies: mining for putative genes involved in parasitism and evaluation of in planta RNAi. PLoS One 10:e0144674. https://doi.org/10.1371/journal.pone.0144674 CrossRefPubMedPubMedCentralGoogle Scholar
  192. Walawage SL, Britton MT, Leslie CA et al (2013) Stacking resistance to crown gall and nematodes in walnut rootstocks. BMC Genomics 14:668. https://doi.org/10.1186/1471-2164-14-668 CrossRefPubMedPubMedCentralGoogle Scholar
  193. Walshe DP, Lehane SM, Lehane MJ (2009) Prolonged gene knockdown in the tsetse fly Glossina by feeding double stranded RNA. Insect Mol Biol 18:11–19PubMedCrossRefPubMedCentralGoogle Scholar
  194. Wang P, Granados RR (2001) Molecular structure of the peritrophic membrane (PM): identification of potential PM target sites for insect control. Arch Insect Biochem Physiol 47:110–118. https://doi.org/10.1002/arch.1041 CrossRefPubMedPubMedCentralGoogle Scholar
  195. Wang Y, Zhang H, Li H et al (2011) Second-generation sequencing supply an effective way to screen RNAi targets in large scale for potential application in pest insect control. PLoS One 6:e18644. https://doi.org/10.1371/journal.pone.0018644 PubMedPubMedCentralCrossRefGoogle Scholar
  196. Wang W, Luo L, Lu H et al (2015) Angiotensin-converting enzymes modulate aphid–plant interactions. Sci Reports 5:8885CrossRefGoogle Scholar
  197. Whyard S, Singh AD, Wong S (2009) Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochem Mol Biol 39:824–832. https://doi.org/10.1016/j.ibmb.2009.09.007 CrossRefPubMedPubMedCentralGoogle Scholar
  198. Will T, Vilcinskas A (2015) The structural sheath protein of aphids is required for phloem feeding. Insect Biochem Mol Biol 57:34–40PubMedCrossRefPubMedCentralGoogle Scholar
  199. Winston WM, Molodowitch C, Hunter CP et al (2002) Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295:2456–2459PubMedCrossRefPubMedCentralGoogle Scholar
  200. Winston WM, Sutherlin M, Wright AJ et al (2007) Caenorhabditis elegans SID-2 is required for environmental RNA interference. PNAS 104:10565–10570. https://doi.org/10.1073/pnas.0611282104 PubMedCrossRefPubMedCentralGoogle Scholar
  201. Winter J, Jung S, Keller S et al (2009) Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 11:228–234PubMedCrossRefPubMedCentralGoogle Scholar
  202. Wuriyanghan H, Rosa C, Falk BW (2011) Oral delivery of double-stranded RNAs and siRNAs induces RNAi effects in the potato/tomato psyllid, Bactericera cockerelli. PLoS One 6:e27736PubMedPubMedCentralCrossRefGoogle Scholar
  203. Wynant N, Verlinden H, Breugelmans B et al (2012) Tissue-dependence and sensitivity of the systemic RNA interference response in the desert locust, Schistocerca gregaria. Insect Biochem Mol Biol 42:911–971PubMedCrossRefPubMedCentralGoogle Scholar
  204. Xiao D, Lu YH, Shang QL et al (2015) Gene silencing of two acetylcholinesterases reveals their cholinergic and non-cholinergic functions in Rhopalosiphum padi and Sitobion avenae. Pest Manag Sci 71:523–530PubMedCrossRefPubMedCentralGoogle Scholar
  205. Xiong Y, Zeng H, Zhang Y et al (2013) Silencing the HaHR3 gene by transgenic plant-mediated RNAi to disrupt Helicoverpa armigera development. Int J Biol Sci 9:370–381PubMedPubMedCentralCrossRefGoogle Scholar
  206. Xu HJ, Chen T, Ma XF et al (2013) Genome-wide screening for components of small interfering RNA (siRNA) and micro-RNA (miRNA) pathways in the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Insect Mol Biol 22:635–647. https://doi.org/10.1111/imb.12051 CrossRefPubMedPubMedCentralGoogle Scholar
  207. Xu L, Duan X, Lv Y et al (2014) Silencing of an aphid carboxylesterase gene by use of plant-mediated RNAi impairs Sitobion avenae tolerance of Phoxim insecticides. Transgenic Res 23:389–396PubMedCrossRefPubMedCentralGoogle Scholar
  208. Xue B, Hamamouch N, Li C et al (2013) The 8D05 parasitism gene of Meloidogyne incognita is required for successful infection of host roots. Phytopathology 103:175–181. https://doi.org/10.1094/PHYTO-07-12-0173-R CrossRefPubMedPubMedCentralGoogle Scholar
  209. 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 148:219–222. https://doi.org/10.1016/j.molbiopara.2006.03.013 CrossRefPubMedPubMedCentralGoogle Scholar
  210. Yanagihara K, Tashiro M, Fukuda Y et al (2006) Effects of short interfering RNA against methicillin-resistant Staphylococcus aureus coagulase in vitro and in vivo. J Antimicrob Chemother 57:122–126PubMedCrossRefPubMedCentralGoogle Scholar
  211. Yang J, Han Z (2014) Efficiency of different methods for dsRNA delivery in cotton bollworm (Helicoverpa armigera). J Integr Agric 13:115–123CrossRefGoogle Scholar
  212. Yao J, Rotenberg D, Afsharifar A et al (2013) Development of RNAi methods for Peregrinus maidis, the corn planthopper. PLoS One 8:e370243Google Scholar
  213. Yin C, Jurgenson JE, Hulbert SH (2011) Development of a host-induced RNAi system in the wheat stripe rust fungus Puccinia striiformis f. sp. tritici. Mol Plant-Microbe Interact 24:554–561. https://doi.org/10.1094/MPMI-10-10-0229 CrossRefPubMedPubMedCentralGoogle Scholar
  214. Zamore PD, Tuschl T, Sharp PA (2000) RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21- to 23-nucleotide intervals. Cell 101:25–33PubMedPubMedCentralCrossRefGoogle Scholar
  215. Zha W, Peng X, Chen R et al (2011) Knockdown of midgut genes by dsRNA-transgenic plant-mediated RNA interference in the hemipteran insect Nilaparvata lugens. PLoS One 6:e20504. https://doi.org/10.1371/journal.pone.0020504 CrossRefPubMedPubMedCentralGoogle Scholar
  216. Zhang Y, Lu Z (2015) Peroxiredoxin 1 protects the pea aphid Acyrthosiphon pisum from oxidative stress induced by Micrococcus luteus infection. J Invertebr Pathol 127:115–121PubMedCrossRefPubMedCentralGoogle Scholar
  217. Zhang H, Kolb F, Jaskiewicz L et al (2004) Single processing center models for human Dicer and bacterial RNase III. Cell 118:57–68PubMedCrossRefPubMedCentralGoogle Scholar
  218. Zhang X, Zhang J, Zhu KY (2010) Chitosan/double-stranded RNA nanoparticle-mediated RNA interference to silence chitin synthase genes through larval feeding in the African malaria mosquito (Anopheles gambiae). Insect Mol Biol 19:683–693. https://doi.org/10.1111/j.1365-2583.2010.01029.x CrossRefPubMedPubMedCentralGoogle Scholar
  219. Zhang M, Wang Q, Xu K et al (2011) Production of dsRNA sequences in the host plant is not sufficient to initiate gene silencing in the colonizing oomycete pathogen Phytophthora parasitica. PLoS One 6:e28114. https://doi.org/10.1371/journal.pone.0028114 PubMedPubMedCentralCrossRefGoogle Scholar
  220. Zhang Y, Zhang SZ, Kulye M et al (2012) Silencing of molt-regulating transcription factor gene, CiHR3, affects growth and development of sugarcane stem borer, Chilo infuscatellus. J Insect Sci 12:1–12Google Scholar
  221. Zhang H, Li HC, Miao XX (2013a) Feasibility, limitation and possible solutions of RNAi-based technology for insect pest control. Insect Sci 20:15–30PubMedCrossRefPubMedCentralGoogle Scholar
  222. Zhang X, Liu X, Ma J et al (2013b) Silencing of cytochrome P450 CYP6B6 gene of cotton bollworm (Helicoverpa armigera) by RNAi. Bull Entomol Res 103:584–591PubMedCrossRefPubMedCentralGoogle Scholar
  223. Zhang J, Khan SA, Hasse C et al (2015a) Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science 347:991–994PubMedCrossRefPubMedCentralGoogle Scholar
  224. Zhang X, Mysore K, Flannery E et al (2015b) Chitosan/interfering RNA nanoparticle mediated gene silencing in disease vector mosquito larvae. J Vis Exp 97:52523. https://doi.org/10.3791/52523 CrossRefGoogle Scholar
  225. Zhang J, Khan SA, Heckel DG et al (2017) Next-generation insect-resistant plants: RNAi-mediated crop protection. Trends Biotechnol 35:871–882PubMedCrossRefPubMedCentralGoogle Scholar
  226. Zhao L, Chen J (2013) Double stranded RNA constructs to control ants. US Patent Application Publication No. 2013/0078212Google Scholar
  227. Zhao Y, Yang G, Wang-Pruski G et al (2008) Phyllotreta striolata (Coleoptera, Chrysomelidae): arginine kinase cloning and RNAi-based pest control. Eur J Biochem 105:815–822Google Scholar
  228. Zhou X, Wheeler MM, Oi FM et al (2008) RNA interference in the termite Reticulitermes flavipes through ingestion of double-stranded RNA. Insect Biochem Mol Biol 38:805–815PubMedCrossRefPubMedCentralGoogle Scholar
  229. Zhu F, Xu J, Palli R et al (2011) Ingested RNA interference for managing the populations of the Colorado potato beetle, Leptinotarsa decemlineata. Pest Manag Sci 67:175–182. https://doi.org/10.1002/ps.2048 CrossRefPubMedPubMedCentralGoogle Scholar
  230. Zhu JQ, Liu S, Ma Y et al (2012) Improvement of pest resistance in transgenic tobacco plants expressing dsRNA of an insect-associated gene EcR. PLoS One 7:e38572PubMedPubMedCentralCrossRefGoogle Scholar
  231. Zhuo K, Chen J, Lin B et al (2017) A novel Meloidogyne enterolobii effector MeTCTP promotes parasitism by suppressing programmed cell death in host plants. Mol Plant Pathol 18:45–54. https://doi.org/10.1111/mpp.12374 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Pradeep Kumar Jain
    • 1
  • Ramcharan Bhattacharya
    • 1
  • Deshika Kohli
    • 1
  • Raghavendra Aminedi
    • 1
  • Pawan Kumar Agrawal
    • 1
  1. 1.ICAR-NRC on Plant Biotechnology, IARI CampusNew DelhiIndia

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