Sequence optimization and multiple gene-targeting improve the inhibitory efficacy of exogenous double-stranded RNA against pepper mottle virus in Nicotiana benthamiana

Kamthan A, Chaudhuri A, Kamthan M, Datta A (2015) Small RNAs in plants: recent development and application for crop improvement. Front Plant Sci 6:208 Shin SY, Shin C (2016) Regulatory non-coding RNAs in plants: potential gene resources for the improvement of agricultural traits. Plant Biotechnol Rep 10:35–47 Zhang J, Khan SA, Hasse C, Ruf S, Heckel DG, Bock R (2015) Pest control. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science 347:991–994 Yoon J, Fang M, Lee D, Park M, Kim K-H, Shin C (2021) Double-stranded RNA confers resistance to pepper mottle virus in Nicotiana benthamiana. Appl Biol Chem 64(1):1–8 Park M, Um TY, Jang G, Choi YD, Shin C (2022) Targeted gene suppression through double-stranded RNA application using easy-to-use methods in Arabidopsis thaliana. Appl Biol Chem 65(1):1–8 Dubrovina AS, Kiselev KV (2019) Exogenous RNAs for gene regulation and plant resistance. Int J Mol Sci 20(9):2282 Das PR, Sherif SM (2020) Application of Exogenous dsRNAs-induced RNAi in agriculture: challenges and triumphs. Front Plant Sci 11:946 Christiaens O, Whyard S, Velez AM, Smagghe G (2020) Double-stranded RNA technology to control insect pests: current status and challenges. Front Plant Sci 11:451 Dalakouras A, Wassenegger M, Dadami E, Ganopoulos I, Pappas ML, Papadopoulou K (2020) Genetically modified organism-free RNA interference: exogenous application of RNA molecules in plants. Plant Physiol 182:38–50 Akbar S, Wei Y, Zhang MQ (2022) RNA interference: promising approach to combat plant viruses. Int J Mol Sci 23(10):5312 Konakalla NC, Kaldis A, Berbati M, Masarapu H, Voloudakis AE (2016) Exogenous application of double-stranded RNA molecules from TMV p126 and CP genes confers resistance against TMV in tobacco. Planta 244:961–969 Mitter N, Worrall EA, Robinson KE, Li P, Jain RG, Taochy C, Fletcher SJ, Carroll BJ, Lu GQ, Xu ZP (2017) Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nat Plants 3:16207 Worrall EA, Bravo-Cazar A, Nilon AT, Fletcher SJ, Robinson KE, Carr JP, Mitter N (2019) Exogenous application of RNAi-inducing double-stranded RNA inhibits aphid-mediated transmission of a plant virus. Front Plant Sci 10:265 Rego-Machado CM, Nakasu EYT, Silva JMF, Lucinda N, Nagata T, Inoue-Nagata AK (2020) siRNA biogenesis and advances in topically applied dsRNA for controlling virus infections in tomato plants. Sci Rep 10:22277 Koch A, Biedenkopf D, Furch A, Weber L, Rossbach O, Abdellatef E, Linicus L, Johannsmeier J, Jelonek L, Goesmann A et al (2016) An RNAi-based control of Fusarium graminearum infections through spraying of long dsRNAs involves a plant passage and is controlled by the fungal silencing machinery. PLoS Pathog 12:e1005901 Wang M, Weiberg A, Lin FM, Thomma BP, Huang HD, Jin H (2016) Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nat Plants 2:16151 McLoughlin AG, Wytinck N, Walker PL, Girard IJ, Rashid KY, de Kievit T, Fernando WGD, Whyard S, Belmonte MF (2018) Identification and application of exogenous dsRNA confers plant protection against Sclerotinia sclerotiorum and Botrytis cinerea. Sci Rep 8:7320 Zhang H, Li H, Guan R, Miao X (2015) Lepidopteran insect species-specific, broad-spectrum, and systemic RNA interference by spraying dsRNA on larvae. Entomologia Experimentalis et Applicata 155(3):218–28 Nitnavare RB, Bhattacharya J, Singh S, Kour A, Hawkesford MJ, Arora N (2021) Next generation dsRNA-based insect control: success so far and challenges. Front Plant Sci 12:673576 Sharif MN, Iqbal MS, Alam R, Awan MF, Tariq M, Ali Q, Nasir IA (2022) Silencing of multiple target genes via ingestion of dsRNA and PMRi affects development and survival in Helicoverpa armigera. Sci Rep 12:10405 Jain RG, Fletcher SJ, Manzie N, Robinson KE, Li P, Lu E, Brosnan CA, Xu ZP, Mitter N (2022) Foliar application of clay-delivered RNA interference for whitefly control. Nat Plants 8:535–548 Dhandapani RK, Gurusamy D, Palli SR (2022) Protamine-Lipid-dsRNA nanoparticles improve RNAi efficiency in the fall Armyworm. Spodoptera frugiperda J Agric Food Chem 70:6634–6643 Gan D, Zhang J, Jiang H, Jiang T, Zhu S, Cheng B (2010) Bacterially expressed dsRNA protects maize against SCMV infection. Plant Cell Rep 29:1261–1268 Posiri P, Ongvarrasopone C, Panyim S (2013) A simple one-step method for producing dsRNA from E. coli to inhibit shrimp virus replication. J Virol Methods. 188:64–69 He W, Xu W, Xu L, Fu K, Guo W, Bock R, Zhang J (2020) Length-dependent accumulation of double-stranded RNAs in plastids affects RNA interference efficiency in the Colorado potato beetle. J Exp Bot 71:2670–2677 Hernández-Soto A, Chacón-Cerdas R (2021) RNAi crop protection advances. Int J Mol Sci 22(22):12148 Fang M, Yu J, Kim KH (2021) Pepper mottle virus and its host interactions: current state of knowledge. Viruses 13(10):1930 Vance VB, Moore D, Turpen TH, Bracker A, Hollowell VC (1992) The complete nucleotide sequence of pepper mottle virus genomic RNA: comparison of the encoded polyprotein with those of other sequenced Potyviruses. Virology 191:19–30 Ala-Poikela M, Rajarnaki ML, Valkonen JPT (2019) A novel interaction network used by Potyviruses in virus-host interactions at the protein level. Viruses-Basel 11(12):1158 Liu DS, Shi LD, Han CG, Yu JL, Li DW, Zhang YL (2012) Validation of reference genes for gene expression studies in virus-infected Nicotiana benthamiana using quantitative real-time PCR. Plos ONE 7(9):e46451 Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25:402–408 Morozov SY, Solovyev AG, Kalinina NO, Taliansky ME (2019) Double-stranded RNAs in plant protection against pathogenic organisms and viruses in agriculture. Acta Naturae 11:13–21 Makinen K, Hafren A (2014) Intracellular coordination of Potyviral RNA functions in infection. Front Plant Sci 5:110 Shen W, Shi Y, Dai Z, Wang A (2020) The RNA-dependent RNA polymerase NIb of Potyviruses plays multifunctional, contrasting roles during viral infection. Viruses 12(1):77 Valli AA, Gallo A, Rodamilans B, Lopez-Moya JJ, Garcia JA (2018) The HCPro from the potyviridae family: an enviable multitasking helper component that every virus would like to have. Mol Plant Pathol 19:744–763 Niehl A, Wyrsch I, Boller T, Heinlein M (2016) Double-stranded RNAs induce a pattern-triggered immune signaling pathway in plants. New Phytol 211:1008–1019 Samarskaya VO, Spechenkova N, Markin N, Suprunova TP, Zavriev SK, Love AJ, Kalinina NO, Taliansky M (2022) Impact of exogenous application of Potato Virus Y-specific dsRNA on RNA interference, pattern-triggered immunity and poly(ADP-ribose) metabolism. Int J Mol Sci 23(14):7915 Niehl A, Heinlein M (2019) Perception of double-stranded RNA in plant antiviral immunity. Mol Plant Pathol 20:1203–1210 Semple SL, Au SKW, Jacob RA, Mossman KL, DeWitte-Orr SJ (2022) Discovery and use of long dsRNA mediated RNA interference to stimulate antiviral protection in interferon competent Mammalian cells. 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