Abstract
The fall armyworm (FAW) Spodoptera frugiperda has rapidly spread from the American continent to many other areas and caused serious damage to local agriculture. To explore a more environmentally friendly and effective strategy to control this pest, we developed a dual-effect RNAi system based on baculovirus infection and gene silencing. V-ATPase subunits A and B of FAW (SfvATPaseA and SfvATPaseB) were cloned to construct a recombinant baculoviruses (rBviruses) of Bacmid-dsSfvATPaseA and Bacmid-dsSfvATPaseB with the capacity to produce small interfering RNA. The efficacy of baculovirus-mediated RNAi was evaluated by injection delivery. The results showed that the relative expression levels of SfvATPaseA and SfvATPaseB were significantly suppressed by the constructed rBviruses, with reduction rates of 73.85% and 69.82%, respectively. The inhibition rates of larval body weight and length resulting from RNAi were more than 82% and 40%, respectively. More importantly, these two rBviruses greatly accelerated the larval death of FAW; compared to a bacmid control, the total mortality was two days less. After ten serial passages, both rBviruses exhibited excellent genetic stabilities. These results suggest that the creation of dual-effect biopesticides with both viral infection and gene silencing activities is feasible and prospective.
Similar content being viewed by others
References
Adeyinka OS, Riaz S, Toufiq N, Yousaf I, Bhatti MU, Batcho A, Olajide AA, Nasir IA, Tabassum B (2020) Advances in exogenous RNA delivery techniques for RNAi mediated pest control. Mol Biol Rep 47(8):6309–6319. https://doi.org/10.1007/s11033-020-05666-2
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 25:1322–1326. https://doi.org/10.1038/nbt1359
Bonning BC, Hoover K, Booth TF, Duffey S, Hammock BD (1995) Development of a recombinant baculovirus expressing a modified juvenile hormone esterase with potential for insect control. Arch Insect Biochem Physiol 30:177–194. https://doi.org/10.1002/arch.940300208
Bramlett M, Plaetinck G, Maienfisch P (2020) RNA-based biocontrols-a new paradigm in crop protection. Engineering 6(5):522–527. https://doi.org/10.1016/j.eng.2019.09.008
Braunagel SC, Summers MD (2007) Molecular biology of the baculovirus occlusion-derived virus envelope. Curr Drug Targets 8(10):1084–1095. https://doi.org/10.2174/138945007782151315
Chambers AC, Aksular M, Graves LP, Irons SL, Possee RD, King LA (2018) Overview of the baculovirus expression system. Curr Protoc Protein Sci 91(1):541–546. https://doi.org/10.1002/cpps.47
Chang Y, Liao Y, Jiang X, Wang G, Yang B (2019) Advances in research on Spodoptera frugiperda and its functional genomics. Plant Protection (china) 45(5):1–7
Christiaens O, Niu J, Taning CNT (2020) RNAi in insects: a revolution in fundamental research and pest control. InSects 11(7):415. https://doi.org/10.3390/insects11070415
Das PR, Sherif SM (2020) Application of exogenous dsRNAs induced RNAi in agriculture: challenges and triumphs. Front Plant Sci 11:946. https://doi.org/10.3389/fpls.2020.00946
Ding L, Guo Z, Xu H, Li T, Wang Y, Tao H (2019) The inhibitory effect of Celangulin V on the ATP hydrolytic activity of the complex of V-ATPase subunits A and B in the midgut of Mythimna separata. Toxins 11(2):130. https://doi.org/10.3390/toxins11020130
Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811. https://doi.org/10.1038/35888
Forgac M (1998) Structure, function and regulation of the vacuolar (H+)-ATPases. FEBS Lett 440(3):258–263. https://doi.org/10.1016/S0014-5793(98)01425-2
Gang F, Li X, Yang C, Han L, Qian H, Wei S, Wu W, Zhang J (2020) Synthesis and insecticidal activity evaluation of virtually screened phenylsulfonamides. J Agric Food Chem 68:11665–11671. https://doi.org/10.1021/acs.jafc.0c02153
Guo J, He K, Wang Z (2019) Biological characteristics, trend of fall armyworm Spodoptera frugiperda, and the strategy for management of the pest. J Appl Entomol (china) 56(3):361–369
Harold FM, Kakinuma Y (1985) Primary and secondary transport of cations in bacteria. Ann N Y Acad Sci 456(1):375–383. https://doi.org/10.1111/j.1749-6632.1985.tb14888.x
Holen T, Amarzguioui M, Wiiger MT, Babaie E, Prydz H (2002) Positional effects of short interfering RNAs targeting the human coagulation trigger tissue factor. Nucl Acids Res 30(8):1757–1766. https://doi.org/10.1093/nar/30.8.1757
Ignoffo CM, Wong JFH, Saathoff SG (1999) Mortality and feeding of mid-stadium larvae of Helicoverpa zea and Heliothis virescens fed a wild strain or a recombinant strain of Baculovirus heliothis expressing an insect-specific toxin of the scorpion Leiurus quinquestriatus hebraeus. Appl Entomol Zool 34:279–283. https://doi.org/10.1303/aez.34.279
Joyce AS, John PH Jr (2002) Evaluation of accuracy and precision of adenovirus absorptivity at 260 nm under conditions of complete DNA disruption. Virology 295:284–288. https://doi.org/10.1006/viro.2002.1406
Kenis M, Benelli G, Biondi A, Calatayud P, Day R, Desneux N, Harrison RD, Kriticos D, Rwomushana I, van den Berg J, Verheggen F, Zhang Y, Agboyi LK, Ahissou RB, Ba MN, Bernal J, Bueno AF, Carrière Y, Carvalho GA, Chen X, Cicero L, Plessis H, Early R, Fallet P, Fiaboe KKM, Firake DM, Goergen G, Groot AT, Guedes RNC, Gupta A, Hu G, Huang F, Jaber LR, Malo EA, McCarthy CB, Meagher RL Jr, Mohamed S, Sanchez DM, Nagoshi RN, Nègre N, Niassy S, Ota N, Nyamukondiwa C, Omoto C, Palli SR, Pavela R, Ramirez-Romero R, Rojas JC, Subramanian S, Tabashnik BE, Tay WT, Virla EG, Wang S, Williams T, Zang L, Zhang L, Wu K (2022) Invasiveness, biology, ecology, and management of the fall armyworm. Entomol Gen, Spodoptera frugiperda. https://doi.org/10.1127/entomologia/2022/1659
Kumar P, Pandit SS, Baldwin IT (2012) Tobacco rattle virus vector: a rapid and transient means of silencing Manduca sexta genes by plant mediated RNA interference. PLoS ONE 7(2):e31347. https://doi.org/10.1371/journal.pone.0031347
Kunte N, McGraw E, Bell S, Held D, Avila LA (2020) Prospects, challenges and current status of RNAi through insect feeding. Pest Manag Sci 76(1):26–41. https://doi.org/10.1002/ps.5588
Lelio ID, Barra E, Coppola M, Corrado G, Rao R, Caccia S (2022) Transgenic plants expressing immunosuppressive dsRNA improve entomopathogen efficacy against Spodoptera littoralis larvae. J Pest Sci 95(3):1413–1428. https://doi.org/10.1007/s10340-021-01467-z
Liu X, Liang X, Guo J, Shi X, Merzendorfer H, Zhu KY, Zhang J (2022) V-ATPase subunit a is required for survival and midgut development of Locusta migratoria. Insect Mol Biol 31(1):60–72. https://doi.org/10.1111/imb.12738
Lu L, Qi Z, Li Q, Wu W (2016) Validation of the target protein of insecticidal dihydroagarofuran sesquiterpene polyesters. Toxins 8(3):79. https://doi.org/10.3390/toxins8030079
Lü J, Guo M, Chen S, Noland JE, Guo W, Sang W, Qi Y, Qiu B, Zhang Y, Yang H, Pan H (2020) Double-stranded RNA targeting vATPase B reveals a potential target for pest management of Henosepilachna vigintioctopunctata. Pestic Biochem Physiol 165:104555. https://doi.org/10.1016/j.pestbp.2020.104555
Ma Z, Zhang Y, Li M, Chao Z, Du X, Yan S, Shen J (2022) A first greenhouse application of bacteria-expressed and nanocarrier-delivered RNA pesticide for Myzus persicae control. J Pest Sci. https://doi.org/10.1007/s10340-022-01485-5
Montezano DG, Specht A, Sosa-Gomez DR, Roque-Specht VF, Sousa-Silva JC, Paula-Moraes SV, Peterson JA, Hunt TE (2018) Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. Afr Entomol 26(2):286–300. https://doi.org/10.4001/003.026.0286
Moscardi F (1999) Assessment of the application of baculoviruses for control of Lepidoptera. Annu Rev Entomol 44:257–289. https://doi.org/10.1146/annurev.ento.44.1.257
Muench SP, Rawson S, Eyraud V, Delmas AF, Silva PD, Phillips C, Trinick J, Harrison MA, Gressent F, Huss M (2014) PA1b inhibitor binding to subunits c and e of the vacuolar ATPase reveals its insecticidal mechanism. J Biol Chem 289(23):16399–16408. https://doi.org/10.1074/jbc.M113.541250
Nelson N, Perzov N, Cohen A, Hagai K, Padler V, Nelson H (2000) The cellular biology of proton-motive force generation by V-ATPases. J Exp Biol 203(1):89–95. https://doi.org/10.1242/jeb.203.1.89
Niu J, Taning CNT, Christiaens O, Smagghe G, Wang J (2018) Chapter one-rethink RNAi in insect pest control: challenges and perspectives. Adv Insect Physiol 55:1–17. https://doi.org/10.1016/bs.aiip.2018.07.003
O’Donnell M (2017) The V-ATPase in insect epithelia. J Exp Biol 220(18):3201–3203. https://doi.org/10.1242/jeb.160564
Pancoska P, Moravek Z, Moll UM (2004) Efficient RNA interference depends on global context of the target sequence: quantitative analysis of silencing efficiency using Eulerian graph representation of siRNA. Nucleic Acids Res 32(4):1469–1479. https://doi.org/10.1093/nar/gkh314
Powell ME, Bradish HM, Gatehouse JA, Fitches EC (2017) Systemic RNAi in the small hive beetle Aethina tumida Murray (Coleoptera: Nitidulidae), a serious pest of the European honey bee Apis mellifera. Pest Manag Sci 73(1):53–63. https://doi.org/10.1002/ps.4365
Qiu L, Sun Y, Jiang Z, Yang P, Liu H, Zhou H, Wang X, Zhang W, Lin Y, Ma W (2019) The midgut V-ATPase subunit A gene is associated with toxicity to crystal 2Aa and crystal 1Ca-expressing transgenic rice in Chilo suppressalis. Insect Mol Biol 28(4):520–527. https://doi.org/10.1111/imb.12570
Rahmani S, Bandani AR (2021) A gene silencing of V-ATPase subunit A interferes with survival and development of the tomato leafminer. Tuta Absoluta. Arch Insect Biochem Physiol 106(1):e21753. https://doi.org/10.1002/arch.21753
Ramkumar G, Asokan R, Prasannakumar NR, Kariyanna B, Karthi S, Alwahibi SM, Elshikh MS, Abdel-Megeed A, Ghaith A, Senthil-Nathan S, Kalaivani K, Hunter WB, Krutmuang P (2021) RNA interference suppression of v-ATPase B and juvenile hormone binding protein genes through topically applied dsRNA on tomato leaves: developing biopesticides to control the South American pinworm, Tuta absoluta (Lepidoptera: Gelechiidae). Front Physiol 12:742871. https://doi.org/10.3389/fphys.2021.742871
Sarmah N, Kaldis A, Taning CNT, Perdikis D, Smagghe G, Voloudakis A (2021) dsRNA-mediated pest management of Tuta absoluta is compatible with its biological control agent Nesidiocoris tenuis. InSects 12(4):274. https://doi.org/10.3390/insects12040274
Sato K, Miyata K, Ozawa S, Hasegawa K (2019) Systemic RNAi of V-ATPase subunit B causes molting defect and developmental abnormalities in Periplaneta fuliginosa. Insect Sci 26(4):721–731. https://doi.org/10.1111/1744-7917.12565
Shi X, Liu X, Cooper AMW, Silver K, Merzendorfer H, Zhu KY, Zhang J (2022) Vacuolar (H+)-ATPase subunit c is essential for the survival and systemic RNA interference response in Locusta migratoria. Pest Manag Sci 78(4):1555–1566. https://doi.org/10.1002/ps.6774
Simón O, Palma L, Williams T, López-Ferber M, Caballero P (2012) Analysis of a naturally-occurring deletion mutant of Spodoptera frugiperda multiple nucleopolyhedrovirus reveals sf58 as a new per os infectivity factor of lepidopteran-infecting baculoviruses. J Invertebr Pathol 109(1):117–126. https://doi.org/10.1016/j.jip.2011.10.010
Sun X (2015) History and current status of development and use of viral insecticides in China. Viruses 7(1):306–319. https://doi.org/10.3390/v7010306
Sun Z, Song Y, Yin G, Zhu C, Wen F (2010) HpRNAs derived from different regions of the NIb gene have different abilities to protect tobacco from infection with potato virus Y. J Phytopathol 158(7–8):566–568. https://doi.org/10.1111/j.1439-0434.2009.01650.x
Terenius O, Papanicolaou A, Garbutt JS, Eleftherianos I, Huvenne H, Kanginakudru S et al (2011) RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J Insect Physiol 57(2):231–245. https://doi.org/10.1016/j.jinsphys.2010.11.006
Tomalski MD, Miller LK (1991) Insect paralysis by baculovirus mediated expression of a mite neurotoxin gene. Nature 352:82–85. https://doi.org/10.1038/352082a0
Tsai CH, Wei SC, Lo HR, Chao YC (2019) Baculovirus as versatile vectors for protein display and biotechnological applications. Curr Issues Mol Biol 34(1):231–256. https://doi.org/10.21775/cimb.034.231
Vasanthakumar T, Rubinstein JL (2020) Structure and roles of V-type ATPases. Trends Biochem Sci 45(4):295–307. https://doi.org/10.1016/j.tibs.2019.12.007
Vitavska O, Wieczorek H, Merzendorfer H (2003) A novel role for subunit C in mediating binding of the H+-V-ATPase to the actin cytoskeleton. J Biol Chem 278(20):18499–18505. https://doi.org/10.1074/jbc.M212844200
Volkman LE (2007) Baculovirus infectivity and the actin cytoskeleton. Curr Drug Targets 8(10):1075–1083. https://doi.org/10.2174/138945007782151379
Wan X, Shi M, Xu J, Liu J, Ye H (2021) Interference efficiency and effects of bacterium-mediated RNAi in the fall armyworm (Lepidoptera: Noctuidae). J Insect Sci 21(5):8. https://doi.org/10.1093/jisesa/ieab073
Wei H, Tan S, Yan S, Li Z, Shen J, Liu X (2022) Nanocarrier-mediated transdermal dsRNA-NPF1 delivery system contributes to pest control via inhibiting feeding behavior in Grapholita molesta. J Pest Sci 95(2):983–995. https://doi.org/10.1007/s10340-021-01422-y
Wieczorek H, Beyenbach KW, Huss M, Vitavska O (2009) Vacuolar-type proton pumps in insect epithelia. J Exp Biol 212(11):1611–1619. https://doi.org/10.1242/jeb.030007
Williamson MS, Bass C, Omoto C, Field LM, Carvalho RA (2013) Investigating the molecular mechanisms of organophosphate and pyrethroid resistance in the fall armyworm Spodoptera frugiperda. PLoS ONE 8(4):e62268. https://doi.org/10.1371/journal.pone.0062268
Zhang H, Li H, Miao X (2013) Feasibility, limitation and possible solutions of RNAi-based technology for insect pest control. Insect Sci 20(1):15–30. https://doi.org/10.1111/j.1744-7917.2012.01513.x
Zhu KY, Palli SR (2020) Mechanisms, applications, and challenges of insect RNA interference. Annu Rev Entomol 65:293–311. https://doi.org/10.1146/annurev-ento-011019-025224
Funding
This research was financially supported by the Key Research and Development Program of Shaanxi Province, China (2022NY-061), and Agricultural Science and Technology Innovation Program of Shaanxi Province, China (NYKJ-2022-YL(XN) 21).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interests
The authors declare that they have no conflict of interest.
Additional information
Communicated by Gaelle LE GOFF.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Bai, S., Jin, D., Jiang, Y. et al. Development of a recombinant baculovirus with dual effects to mediate V-ATPase interference by RNA in the fall armyworm Spodoptera frugiperda. J Pest Sci 96, 1667–1681 (2023). https://doi.org/10.1007/s10340-023-01626-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-023-01626-4