DOI QR코드

DOI QR Code

Insect Pest Control Technique Using dsRNA

dsRNA를 이용한 해충방제 기술

  • Kim, Yonggyun (Department of Plant Medicals, Andong National University)
  • Received : 2017.02.25
  • Accepted : 2017.04.15
  • Published : 2017.06.01

Abstract

Gene silencing using double-stranded RNA (dsRNA) has been widely used in functional genomics in biological organisms. Its principle stems from RNA interference (RNAi), a post-transcriptional control of gene expression. Suppression of specific gene expression using dsRNA may give significant lethal effect. Insect pest control exploits this molecular process to develop novel insecticides using specific dsRNAs. This review explains core principles of RNAi using dsRNA. Then it illustrates various examples to control insect pests using dsRNAs. It also discusses limitations to control insect pests using dsRNAs. Finally, it provides several breakthroughs to develop dsRNA insecticides.

Acknowledgement

Supported by : 농촌진흥청

References

  1. Airs, P.M., Bartholomay, L.C., 2017. RNA interference for mosquito and mosquito-borne disease control. Insects 8, 4. https://doi.org/10.3390/insects8010004
  2. Araujo, R.N., Santos, A., Pinto, F.S., Gontijo, N.F., Lehane, M.J., Pereira, M.H., 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, 683-693. https://doi.org/10.1016/j.ibmb.2006.05.012
  3. Attasart, P., Namramoon, O., Kongphom, U., Chimwai, C., Panyim, S., 2013. Ingestion of bacteria expressing dsRNA triggers specific RNA silencing in shrimp. Virus Res. 171, 252-256. https://doi.org/10.1016/j.virusres.2012.11.012
  4. Bass, C., Denholm, I., Williamson, M.S., Nauen, R., 2015. The global status of insect resistance to neonicotinoid insecticides. Pestic. Biochem. Physiol. 121, 78-87. https://doi.org/10.1016/j.pestbp.2015.04.004
  5. Baum, J.A., Bogaert, T., Clinton, W., Heck, G.R., 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
  6. Behura, S.K., 2007. Insect microRNAs: structure, function and evolution. Insect Biochem. Mol. Biol. 37, 3-9. https://doi.org/10.1016/j.ibmb.2006.10.006
  7. Boisson, B., Jacques, J.C., Choumet, V., Martin, E., Xu, J.N., Vernick, K., Bourgouin, C., 2006. Gene silencing in mosquito salivary glands by RNAi. FEBS Lett. 580, 1988-1992. https://doi.org/10.1016/j.febslet.2006.02.069
  8. Bologna, N.G., Voinnet, O., 2014. The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu. Rev. Plant Biol. 65, 473-503. https://doi.org/10.1146/annurev-arplant-050213-035728
  9. Bucher, G., Scholten, J., Klingler, M., 2002. Parental RNAi in Tribolium (Coleoptera). Curr. Biol. 12, R85-R86. https://doi.org/10.1016/S0960-9822(02)00666-8
  10. Chikate, Y.R., Dawkar, V.V., Barbole, R.S., Tilak, P.V., Gupta, V.S., Giri, A.P., 2016. RNAi of selected candidate genes interrupts growth and development of Helicoverpa armigera. Pestic. Biochem. Physiol. 133, 44-51. https://doi.org/10.1016/j.pestbp.2016.03.006
  11. Dzitoyeva, S., Dimitrijevic, N., Manev, H., 2001. Intra-abdominal injection of double-stranded RNA into anesthetized adult Drosophila triggers RNA interference in the central nervous system. Mol. Psychiatry 6, 665-670. https://doi.org/10.1038/sj.mp.4000955
  12. Fire, A., Xu, S.Q., Montgomery, M.K., Kostas, S.A., Driver, S.E., Mello, C.C., 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811. https://doi.org/10.1038/35888
  13. Fishilevich, E., Vélez, A.M., Khajuria, C., Frey, M.L., Hamm, R.L., Wang, H., Schulenberg, G.A., Bowling, A.J., Pence, H.E., Gandra, P., Arora, K., Storer, N.P., Narva, K.E., Siegfried, B.D., 2016. Use of chromatin remodeling ATPases as RNAi targets for parental control of western corn rootworm (Diabrotica virgifera virgifera) and Neotropical brown stink bug (Euschistus heros). Insect Biochem. Mol. Biol. 71, 58-71. https://doi.org/10.1016/j.ibmb.2016.02.004
  14. Ganbaatar, O., Cao, B., Zhang, Y., Bao, D., Bao, W., Wuriyanghan, H., 2017. Knockdown of Mythimna separata chitinase genes via bacterial expression and oral delivery of RNAi effectors. BMC Biotechnol. 17, 9. https://doi.org/10.1186/s12896-017-0328-7
  15. Gong, L., Chen, Y., Hu, Z., Hu, M., 2013. Testing insecticidal activity of novel chemically synthesized siRNA against Plutella xylostella under laboratory and field conditions. PLoS One 8, e62990. https://doi.org/10.1371/journal.pone.0062990
  16. Gordon, K.H.J., Waterhouse, P.M., 2007. RNAi for insect-proof plants. Nat. Biotechnol. 25, 1231-1232. https://doi.org/10.1038/nbt1107-1231
  17. Griebler, M., Westerlund, S.A., Hoffmann, K.H., Meyering-Vos, M., 2008. RNA interference with the allatoregulating neuropeptide genes from the fall armyworm Spodoptera frugiperda and its effects on the JH titer in the hemolymph. J. Insect Physiol. 54, 997-1007. https://doi.org/10.1016/j.jinsphys.2008.04.019
  18. Guan, R., Li, H., Miao, X., 2017. RNAi pest control and enhanced Bt insecticidal efficiency achieved by dsRNA of chymotrypsinlike genes in Ostrinia furnacalis. J. Pest. Sci. 90, 745-757. https://doi.org/10.1007/s10340-016-0797-9
  19. Hakim, R.S., Baldwin, K., Smagghe, G., 2010. Regulation of midgut growth, development, and metamorphosis. Annu. Rev. Entomol. 55, 593-608. https://doi.org/10.1146/annurev-ento-112408-085450
  20. 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
  21. Jayachandran, B., Hussain, M., Asgari, S., 2013. An insect trypsinlike serine protease as a target of microRNA: utilization of microRNA mimics and inhibitors by oral feeding. Insect Biochem. Mol. Biol. 43, 398-406. https://doi.org/10.1016/j.ibmb.2012.10.004
  22. Jose, A.M., Smith, J.J., Hunter, C.P., 2009. Export of RNA silencing from C. elegans tissues does not require the RNA channel SID-1. Proc. Natl. Acad. Sci. USA 106, 2283-2288.
  23. Kamath, R.S., Ahringer, J., 2003. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313-321. https://doi.org/10.1016/S1046-2023(03)00050-1
  24. Kennerdell, J.R., Carthew, R.W., 1998. Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway. Cell 95, 1017-1026. https://doi.org/10.1016/S0092-8674(00)81725-0
  25. Khajuria, C., Vélez, A.M., Rangasamy, M., Wang, H., Fishilevich, E., Frey, M.L., Carneiro, N.P., Gandra, P., Narva, K.E., Siegfried, B.D., 2015. Parental RNA interference of genes involved in embryonic development of the western corn rootworm, Diabrotica virgifera virgifera LeConte. Insect Biochem. Mol Biol. 63, 54-62. https://doi.org/10.1016/j.ibmb.2015.05.011
  26. Kim, Y., 2014. Development and application of novel biopesticides using insect immunosuppression, in Park, Y.M., Chun, I.J., Kim, Y., Lim, U.T., Lim, J.H. (Eds.), Horticultural crops: development and application of novel technologies. ANU Ag. Sci. Tech. Institute, Andong, pp. 41-112.
  27. Kim, E., Kim, Y., 2016. A freeze-drying formulation and target specificity of double-stranded RNA-expressing bacteria to control insect pests. Korean J. Appl. Entomol. 55, 81-89.
  28. Kim, E., Park, Y., Kim, Y., 2015a. A transformed bacterium expressing double-stranded RNA specific to integrin ${\beta}1$ enhances Bt toxin efficacy against a polyphagous insect pest, Spodoptera exigua. PLoS One 10, e0132631. https://doi.org/10.1371/journal.pone.0132631
  29. Kim, Y., Kim, E., Park, Y., Kim, Y., 2015b. Construction of a transgenic tobacco expressing a polydnaviral cystatin. Korean J. Appl. Entomol. 54, 1-9. https://doi.org/10.5656/KSAE.2015.01.1.055
  30. Kim, Y.H., Issa, M.S., Cooper, A.M.W., Zhu, K.Y., 2015c. RNA interference: applications and advances in insect toxicology and insect pest management. Pesti. Biochem. Physiol. 120, 109-117. https://doi.org/10.1016/j.pestbp.2015.01.002
  31. Kim, H.S., Noh, S., Park, Y., 2017. Enhancement of Bacillus thuringiensis Cry1Ac and Cry1Ca toxicity against Spodoptera exigua (Hübner) by suppression of a chitin synthase B gene in midgut. J. Asia Pac. Entomol. 20, 199-205. https://doi.org/10.1016/j.aspen.2016.12.015
  32. Kühn, L.C., 2015. Iron regulatory proteins and their role in controlling iron metabolism. Metallomics 7, 232-243 https://doi.org/10.1039/C4MT00164H
  33. Li, X., Zhang, M., Zhang, H., 2011. RNA interference of four genes in adult Bactrocera dorsalis by feeding their dsRNAs. PLoS One 6, e17788. https://doi.org/10.1371/journal.pone.0017788
  34. Lim, Z.X., Robinson, K.E., Jain, R.G., Chandra, G.S., Asokan, R., Asgari, S., Mitter, N., 2016. Diet-delivered RNAi in Helicoverpa armigera - progresses and challenges. J. Insect Physiol. 85, 86-93. https://doi.org/10.1016/j.jinsphys.2015.11.005
  35. Ling, L., Ge, X., Li, Z., Zeng, B., Xu, J., Chen, X., Shang, P., James, A.A., Huang, Y., Tan, A., 2015. MiR-2 family targets awd and fng to regulate wing morphogenesis in Bombyx mori. RNA Biol. 12, 742-748. https://doi.org/10.1080/15476286.2015.1048957
  36. Mansoori, B., Sandoghchian Shotorbani, S., Baradaran, B., 2014. RNA interference and its role in cancer therapy. Adv. Pharm. Bull. 4, 313-321.
  37. Mao, Y.B., Cai, W.J., Wang, J.W., Hong, G.J., Tao, X.Y., Wang, L.J., Huang, Y.P., Chen, X.Y., 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
  38. Mao, Y.B., Tao, X.Y., Xue, X.Y., Wang, L.J., Chen, X.Y., 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
  39. Mao, J., Zhang, P., Liu, C., Zeng, F., 2015. Co-silence of the coatomer ${\beta}$ and v-ATPase A genes by siRNA feeding reduces larval survival rate and weight gain of cotton bollworm, Helicoverpa armigera. Pestic. Biochem. Physiol. 118, 71-76. https://doi.org/10.1016/j.pestbp.2014.11.013
  40. Meyering-Vos, M., Muller, A. 2007. RNA interference suggests sulfakinins as satiety effectors in the cricket Gryllus bimaculatus. J. Insect Physiol. 53, 840-848. https://doi.org/10.1016/j.jinsphys.2007.04.003
  41. Miller, S.C., Brown, S.J., Tomoyasu, Y., 2008. Larval RNAi in Drosophila? Dev. Genes Evol. 218, 505-510. https://doi.org/10.1007/s00427-008-0238-8
  42. Pearson, A., Lux, A., Krieger, M., 1995. Expression cloning of DSR-CI, a class-C macrophage-specific scavenger receptor from Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 92, 4056-4060.
  43. Price, D.R.G., Gatehouse, J.A., 2008. RNAi-mediated crop protection against insects. Trends Biotechnol. 26, 393-400. https://doi.org/10.1016/j.tibtech.2008.04.004
  44. Roignant, J.Y., Carre, C., Mugat, R., Szymczak, D., Lepesant, J.A., Antoniewski, C., 2003. Absence of transitive and systemic pathways allows cell-specific and isoform specific RNAi in Drosophila. RNA 9, 299-308. https://doi.org/10.1261/rna.2154103
  45. Runo, S., Alakonya, A., Machuka, J., Sinha, N., 2011. RNA interference as a resistance mechanism against crop parasites in Africa: a "Trojan horse' approach. Pest. Manag. Sci. 67, 129-136. https://doi.org/10.1002/ps.2052
  46. Saleh, M.C., van Rij, R.P., Hekele, A., Gillis, A., Foley, E., O'Farrell, P.H., Andino, R., 2006. The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nature Cell Biol. 8, 793-802. https://doi.org/10.1038/ncb1439
  47. Saleh, M.C., Tassetto, M., van Rij, R.P., Goic, B., Gausson, V., Berry, B., Jacquier, C., Antoniewski, C., Andino, R., 2009. Antiviral immunity in Drosophila requires systemic RNA interference spread. Nature 458, 346-351. https://doi.org/10.1038/nature07712
  48. Scott, J.G., Michel, K., Bartholomay, L.C., Siegfried, B.D., Hunter, W.B., Smagghe, G., Zhu, K.Y., Douglas, A.E., 2013. Towards the elements of successful insect RNAi. J. Insect Physiol. 59, 1212-1221. https://doi.org/10.1016/j.jinsphys.2013.08.014
  49. Shakesby, A.J., Wallace, I.S., Isaacs, H.V., Pritchard, J., Roberts, D.M., Douglas, A.E., 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
  50. Sivakumar, S., Rajagopal, R., Venkatesh, G.R., Srivastava, A., Bhatnagar, R.K., 2007. Knockdown of aminopeptidase-N from Helicoverpa armigera larvae and in transfected Sf21 cells by RNA interference reveals its functional interaction with Bacillus thuringiensis insecticidal protein Cry1Ac. J. Biol. Chem. 282, 7312-7319. https://doi.org/10.1074/jbc.M607442200
  51. Spit, J., Philips, A., Wynant, N., Santos, D., Plaetinck, G., Vanden Broeck, J., 2017. Knockdown of nuclease activity in the gut enhances RNAi efficiency in the Colorado potato beetle, Leptinotarsa decemlineata, but not in the desert locust, Schistocerca gregaria. Insect Biochem. Mol. Biol. 81, 103-116. https://doi.org/10.1016/j.ibmb.2017.01.004
  52. Sugahara, R., Tanaka, S., Jouraku, A., Shiotsuki, T., 2017. Geographic variation in RNAi sensitivity in the migratory locust. Gene 605, 5-11. https://doi.org/10.1016/j.gene.2016.12.028
  53. Terenius, O., Papanicolaou, A., Garbutt, J.S., Eleftherianos, I., Huvenne, H., Kanginakudru, S., Albrechtsen, M., An, C., Aymeric, J.L., Barthel, A., Bebas, P., Bitra, K., Bravo, A., Chevalier, F., Collinge, D.P., Crava, C.M., de Maagd, R.A., Duvic, B., Erlandson, M., Faye, I., Felfoldi, G., Fujiwara, H., Futahashi, R., Gandhe, A.S., Gatehouse, H.S., Gatehouse, L.N., Giebultowicz, J.M., Gomez, I., Grimmelikhuijzen, C.J., Groot, A.T., Hauser, F., Heckel, D.G., Hegedus, D.D., Hrycaj, S., Huang, L., Hull, J.J., Iatrou, K., Iga, M., Kanost, M.R., Kotwica, J., Li, C., Li, J., Liu, J., Lundmark, M., Matsumoto, S., Meyering-Vos, M., Millichap, P.J., Monteiro, A., Mrinal, N., Niimi, T., Nowara, D., Ohnishi, A., Oostra, V., Ozaki, K., Papakonstantinou, M., Popadic, A., Rajam, M.V., Saenko, S., Simpson, R.M., Soberon, M., Strand, M.R., Tomita, S., Toprak, U., Wang, P., Wee, C.W., Whyard, S., Zhang, W., Nagaraju, J., Ffrench-Constant, R.H., Herrero, S., Gordon, K., Swevers, L., Smagghe, G., 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
  54. Tian, H., Peng, H., Yao, Q., Chen, H., Xie, Q., Tang, B., Zhang, W., 2009. Developmental control of a lepidopteran pest Spodoptera exigua by ingestion of bacteria expressing dsRNA of a non-midgut gene. PLoS One 4, e6225. https://doi.org/10.1371/journal.pone.0006225
  55. Timmons, L., Fire, A., 1998. Specific interference by ingested dsRNA. Nature 395, 854. https://doi.org/10.1038/27579
  56. Timmons, L., Court, D.L., 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
  57. Tomoyasu, Y., Denell, R.E., 2004. Larval RNAi in Tribolium (Coleoptera) for analyzing adult development. Dev. Genes Evol. 214, 575-578. https://doi.org/10.1007/s00427-004-0434-0
  58. Tomoyasu, Y., Miller, S.C., Tomita, S., Schoppmeier, M., Grossmann, D., Bucher, G., 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
  59. Ulvila, J., Parikka, M., Kleino, A., Sormunen, R., Ezekowitz, R.A., Kocks, C., Ramet, M., 2006. Double-stranded RNA is internalized by scavenger receptor-mediated endocytosis in Drosophila S2 cells. J. Biol. Chem. 281, 14370-14375. https://doi.org/10.1074/jbc.M513868200
  60. Velez, A.M., Khajuria, C., Wang, H., Narva, K.E., Siegfried, B.D., 2016. Knockdown of RNA interference pathway genes in Western corn rootworms (Diabrotica virgifera virgifera Le Conte) demonstrates a possible mechanism of resistance to lethal dsRNA. PLoS One 11, e0157520. https://doi.org/10.1371/journal.pone.0157520
  61. Volz, J., Muller, H.M., Zdanowicz, A., Kafatos, F.C., Osta, M.A., 2006. A genetic module regulates the melanization response of Anopheles to Plasmodium. Cell. Microbiol. 8, 1392-1405. https://doi.org/10.1111/j.1462-5822.2006.00718.x
  62. Whangbo, J.S., Hunter, C.P., 2008. Environmental RNA interference. Trends Genet. 24, 297-305. https://doi.org/10.1016/j.tig.2008.03.007
  63. Winston, W.M., Molodowitch, C., Hunter, C.P., 2002. Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295, 2456-2459. https://doi.org/10.1126/science.1068836
  64. Winston, W.M., Sutherlin, M., Wright, A.J., Feinberg, E.H., Hunter, C.P., 2007. Caenorhabditis elegans SID-2 is required for environmental RNA interference. Proc. Natl. Acad. Sci. USA 104, 10565-10570.
  65. Wynant, N., Santos, D., Van Wielendaele, P., Vanden Broeck, J. 2014. Scavenger receptor-mediated endocytosis facilitates RNA interference in the desert locust, Schistocerca gregaria. Insect Mol. Biol. 23, 320-329.
  66. Xiao, D., Gao, X., Xu, J., Liang, X., Li, Q., Yao, J., Zhu, K.Y., 2015. Clathrin-dependent endocytosis plays a predominant role in cellular uptake of double-stranded RNA in the red flour beetle. Insect Biochem. Mol. Biol. 60, 68-77. https://doi.org/10.1016/j.ibmb.2015.03.009
  67. Xiong, Y., Zeng, H., Zhang, Y., Xu, D., Qiu, D., 2013. Silencing the HaHR3 gene by transgenic plant-mediated RNAi to disrupt Helicoverpa armigera development. Intl. J. Biol. Sci. 9, 370-381. https://doi.org/10.7150/ijbs.5929
  68. Xu, J., Wang, X.F., Chen, P., Liu, F.T., Zheng, S.C., Ye, H., Mo, M.H., 2016. RNA interference in moths: mechanisms, applications, and progress. Genes 7, 88. https://doi.org/10.3390/genes7100088
  69. Yu, N., Christiaens, O., Liu, J., Niu, J., Cappelle, K., Caccia, S., Huvenne, H., Smagghe, G., 2013. Delivery of dsRNA for RNAi in insects: an overview and future directions. Insect Sci. 20, 4-14. https://doi.org/10.1111/j.1744-7917.2012.01534.x
  70. Zha, W., Peng, X., Chen, R., Du, B., Zhu, L., He, G., 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
  71. Zhang, X., Zhang, J., Zhu, K.Y., 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
  72. Zhang, H., Li, H.C., Miao, X.X., 2013. Feasibility, limitation and possible solutions of RNAi-based technology for insect pest control. Insect Sci. 20, 15-30. https://doi.org/10.1111/j.1744-7917.2012.01513.x
  73. Zhou, X., Wheeler, M.M., Oi, F.M., Scharf, M.E., 2008. RNA interference in the termite Reticulitermes flavipes through ingestion of double-stranded RNA. Insect Biochem. Mol. Biol. 38, 805-815. https://doi.org/10.1016/j.ibmb.2008.05.005
  74. Zhu, F., Xu, J., Palli, R., Ferguson, J., Palli, S.R., 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
  75. Zhu, J.Q., Liu, S., Ma, Y., Zhang, J.Q., Qi, H.S., Wei, Z.J., Yao, Q, Zhang, WQ, Li, S., 2012. Improvement of pest resistance in transgenic tobacco plants expressing dsRNA of an insectassociated gene EcR. PLoS One 7, e38572. https://doi.org/10.1371/journal.pone.0038572
  76. Nauen, R., 2006. Insecticide mode of action: return of the ryanodine receptor. Pest Manage. Sci. 62, 690-692. https://doi.org/10.1002/ps.1254