RNA interference: Applications and advances in insect toxicology and insect pest management

Pesticide Biochemistry and Physiology

Volumn 120, Issue , 2015, Pages 109-117

  Kim, Young Ho ^a   Soumaila Issa, Moustapha ^a   Cooper, Anastasia M W ^a   Zhu, Kun Yan ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

Detoxification; Insect toxicology; Insecticide resistance; Pest management; RNA interference

Indexed keywords

BACILLUS THURINGIENSIS; HEXAPODA;

INSECT PROTEIN;

ANIMAL; BIOLOGICAL PEST CONTROL; GENETICS; INSECT; RNA INTERFERENCE;

ANIMALS; INSECT PROTEINS; INSECTS; PEST CONTROL, BIOLOGICAL; RNA INTERFERENCE;

EID: 84927769894     PISSN: 00483575     EISSN: 10959939     Source Type: Journal    
DOI: 10.1016/j.pestbp.2015.01.002     Document Type: Review

References (86)

1. Sen G.L., Blau H.M. A brief history of RNAi: the silence of the genes. FASEB J. 2006, 20:1293-1299.
2. Zhang H., Li H.C., Miao X.X. Feasibility, limitation and possible solutions of RNAi-based technology for insect pest control. Insect Sci 2013, 20:15-30.
3. Gu L.Q., Knipple D.C. Recent advances in RNA interference research in insects: implications for future insect pest management strategies. Crop Prot 2013, 45:36-40.
4. Scott J.G., Michel K., Bartholomay L.C., Siegfried B.D., Hunter W.B., Smagghe G., et al. Towards the elements of successful insect RNAi. J. Insect Physiol 2013, 59:1212-1221.
5. Yu N., Christiaens O., Liu J.S., Niu J.Z., Cappelle K., Caccia S., et al. Delivery of dsRNA for RNAi in insects: an overview and future directions. Insect Sci 2013, 20:4-14.
6. Zhu K.Y. RNA interference: a powerful tool in entomological research and a novel approach for insect pest management PREFACE. Insect Sci 2013, 20:1-3.
7. Perrimon N., Ni J.Q., Perkins L. In vivo RNAi: today and tomorrow. Cold Spring Harb. Perspect. Biol 2010, 2:a003640.
8. Mohr S.E., Perrimon N. RNAi screening: new approaches, understandings, and organisms. Wiley Interdiscip. Rev. RNA 2012, 3:145-158.
9. Hammond S.M. Dicing and slicing: the core machinery of the RNA interference pathway. FEBS Lett 2005, 579:5822-5829.
10. Huvenne H., Smagghe G. Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J. Insect Physiol 2010, 56:227-235.
11. Koch A., Kogel K.H. New wind in the sails: improving the agronomic value of crop plants through RNAi-mediated gene silencing. Plant Biotechnol. J. 2014, 12:821-831.
12. He G.L., Sun Y., Li F. RNA interference of two acetylcholinesterase genes in Plutella xylostella reveals their different functions. Arch. Insect Biochem. Physiol 2012, 79:75-86.
13. Kumar M., Gupta G.P., Rajam M.V. Silencing of acetylcholinesterase gene of Helicoverpa armigera by siRNA affects larval growth and its life cycle. J. Insect Physiol 2009, 55:273-278.
14. Lu Y.H., Park Y., Gao X.W., Zhang X., Yao J.X., Pang Y.P., et al. Cholinergic and non-cholinergic functions of two acetylcholinesterase genes revealed by gene-silencing in Tribolium castaneum. Sci. Rep 2012, 2:288.
15. Revuelta L., Piulachs M.D., Belles X., Castanera P., Ortego F., Diaz-Ruiz J.R., et al. RNAi of ace1 and ace2 in Blattella germanica reveals their differential contribution to acetylcholinesterase activity and sensitivity to insecticides. Insect Biochem. Mol. Biol 2009, 39:913-919.
16. Hui X.M., Yang L.W., He G.L., Yang Q.P., Han Z.J., Li F. RNA interference of ace1 and ace2 in Chilo suppressalis reveals their different contributions to motor ability and larval growth. Insect Mol. Biol 2011, 20:507-518.
17. Rinkevich F.D., Scott J.G. Limitations of RNAi of a6 nicotinic acetylcholine receptor subunits for assessing the in vivo sensitivity to spinosad. Insect Sci 2013, 20:101-108.
18. A receptor RDL inhibits Drosophila olfactory associative learning. Neuron 2007, 56:1090-1102.
19. Wan P.J., Guo W.Y., Yang Y., Lu F.G., Lu W.P., Li G.Q. RNAi suppression of the ryanodine receptor gene results in decreased susceptibility to chlorantraniliprole in Colorado potato beetle Leptinotarsa decemlineata. J. Insect Physiol 2014, 63:48-55.
20. Yang Y., Wan P.J., Hu X.X., Li G.Q. RNAi mediated knockdown of the ryanodine receptor gene decreases chlorantraniliprole susceptibility in Sogatella furcifera. Pestic. Biochem. Physiol 2014, 108:58-65.
21. Khajuria C., Buschman L.L., Chen M.S., Siegfried B.D., Zhu K.Y. Identification of a novel aminopeptidase P-like gene (OnAPP) possibly involved in Bt toxicity and resistance in a major corn pest (Ostrinia nubilalis). PLoS ONE 2011, 6:e23983.
22. Rajagopal R., Sivakumar S., Agrawal N., Malhotra P., Bhatnagar R.K. Silencing of midgut aminopeptidase N of Spodoptera litura by double-stranded RNA establishes its role as Bacillus thuringiensis toxin receptor. J. Biol. Chem 2002, 277:46849-46851.
23. Ren X.L., Chen R.R., Zhang Y., Ma Y., Cui J.J., Han Z.J., et al. A Spodoptera exigua Cadherin serves as a putative receptor for Bacillus thuringiensis Cry1Ca toxin and shows differential enhancement of Cry1Ca and Cry1Ac toxicity. Appl. Environ. Microbiol 2013, 79:5576-5583.
24. Massoulie J., Pezzementi L., Bon S., Krejci E., Vallette F.M. Molecular and cellular biology of cholinesterases. Prog. Neurobiol 1993, 41:31-91.
25. Baek J.H., Kim J.I., Lee D.W., Chung B.K., Miyata T., Lee S.H. Identification and characterization of ace1-type acetylcholine sterase likely associated with organophosphate resistance in Plutella xylostella. Pestic. Biochem. Physiol 2005, 81:164-175.
26. Kim J.I., Jung C.S., Koh Y.H., Lee S.H. Molecular, biochemical and histochemical characterization of two acetylcholinesterase cDNAs from the German cockroach Blattella germanica. Insect Mol. Biol 2006, 15:513-522.
27. Kim Y.H., Kwon D.H., Lee S.H. Characterization of two distinct acetylcholinesterases possessing almost identical catalytic activity in a damselfly, Vestalis gracilis. J. Asia Pac. Entomol 2013, 16:465-471.
28. Kim Y.H., Lee S.H. Which acetylcholinesterase functions as the main catalytic enzyme in the Class Insecta?. Insect Biochem. Mol. Biol 2013, 43:47-53.
29. Lee D.W., Kim S.S., Shin S.W., Kim W.T., Boo K.S. Molecular characterization of two acetylcholinesterase genes from the oriental tobacco budworm, Helicoverpa assulta (Guenee). Biochim. Biophys. Acta 2006, 1760:125-133.
30. Lee S.W., Kasai S., Komagata O., Kobayashi M., Agui N., Kono Y., et al. Molecular characterization of two acetylcholinesterase cDNAs in Pediculus human lice. J. Med. Entomol 2007, 44:72-79.
31. Kim Y.H., Choi J.Y., Je Y.H., Koh Y.H., Lee S.H. Functional analysis and molecular characterization of two acetylcholinesterases from the German cockroach, Blattella germanica. Insect Mol. Biol 2010, 19:765-776.
32. Seong K.M., Kim Y.H., Kwon D.H., Lee S.H. Identification and characterization of three cholinesterases from the common bed bug, Cimex lectularius. Insect Mol. Biol 2012, 21:149-159.
33. Alon M., Alon F., Nauen R., Morin S. Organophosphates resistance in the B-biotype of Bemisia tabaci (Hemiptera: Aleyrodidae) is associated with a point mutation in an ace1-type acetylcholinesterase and overexpression of carboxylesterase. Insect Biochem. Mol. Biol 2008, 38:940-949.
34. Nabeshima T., Mori A., Kozaki T., Iwata Y., Hidoh O., Harada S., et al. An amino acid substitution attributable to insecticide-insensitivity of acetylcholinesterase in a Japanese encephalitis vector mosquito, Culex tritaeniorhynchus. Biochem. Biophys. Res. Commun 2004, 313:794-801.
35. Oh S.H., Kozaki T., Mizuno H., Tomita T., Kono Y. Expression of Ace-paralogous acetylcholinesterase of Culex tritaeniorhynchus with an amino acid substitution conferring insecticide insensitivity in baculovirus-insect cell system. Pestic. Biochem. Physiol 2006, 85:46-51.
36. Weill M., Lutfalla G., Mogensen K., Chandre F., Berthomieu A., Berticat C., et al. Insecticide resistance in mosquito vectors. Nature 2003, 423:136-137.
37. Kim Y.H., Cha D.J., Jung J.W., Kwon H.W., Lee S.H. Molecular and kinetic properties of two acetylcholinesterases from the Western honey bee, Apis mellifera. PLoS ONE 2012, 7:e48838.
38. Cao Y.Q., Liu L.H., Wang J.M., Wang Y.H., Shen W.D., Li B. Functional study of acetylcholinesterase genes in Bombyx mori ovary cells using RNA interference. Entomol. Exp. Appl 2012, 142:140-144.
39. Raymond-Delpech V., Matsuda K., Sattelle B.M., Rauh J.J., Sattelle D.B. Ion channels: molecular targets of neuroactive insecticides. Invert. Neurosci 2005, 5:119-133.
40. Perry T., McKenzie J.A., Batterham P. A Dalpha6 knockout strain of Drosophila melanogaster confers a high level of resistance to spinosad. Insect Biochem. Mol. Biol 2007, 37:184-188.
41. Sattelle D.B., Cordova D., Cheek T.R. Insect ryanodine receptors: molecular targets for novel pest control chemicals. Invert. Neurosci 2008, 8:107-119.
42. Hardy M.C. Resistance is not futile: it shapes insecticide discovery. Insects 2014, 5:227-242.
43. Hu Z., Lin Q., Chen H., Li Z., Yin F., Feng X. Identification of a novel cytochrome P450 gene, CYP321E1 from the diamondback moth, Plutella xylostella (L.) and RNA interference to evaluate its role in chlorantraniliprole resistance. Bull. Entomol. Res 2014, 104:716-723.
44. Zhang J.Q., Li D.Q., Ge P.T., Yang M.L., Guo Y.P., Zhu K.Y., et al. RNA interference revealed the roles of two carboxylesterase genes in insecticide detoxification in Locusta migratoria. Chemosphere 2013, 93:1207-1215.
45. Guo Y.Q., Zhang J.Z., Yu R.R., Zhu K.Y., Guo Y.P., Ma E.B. Identification of two new cytochrome P450 genes and RNA interference to evaluate their roles in detoxification of commonly used insecticides in Locusta migratoria. Chemosphere 2012, 87:709-717.
46. Mao Y.B., Cai W.J., Wang J.W., Hong G.J., Tao X.Y., Wang L.J., et al. Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat. Biotechnol 2007, 25:1307-1313.
47. Bautista M.A., Miyata T., Miura K., Tanaka T. RNA interference-mediated knockdown of a cytochrome P450, CYP6BG1, from the diamondback moth, Plutella xylostella, reduces larval resistance to permethrin. Insect Biochem. Mol. Biol 2009, 39:38-46.
48. Xu L.J., Duan X.L., Lv Y.H., Zhang X.H., Nie Z.S., Xie C.J., et al. Silencing of an aphid carboxylesterase gene by use of plant-mediated RNAi impairs Sitobion avenae tolerance of Phoxim insecticides. Transgenic Res 2014, 23:389-396.
49. Gong Y.H., Yu X.R., Shang Q.L., Shi X.Y., Gao X.W. 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 2014, 9:e102823.
50. Zhang J.Z., Zhang J.Q., Yang M.L., Jia Q.D., Guo Y.P., Ma E.B., et al. Genomics-based approaches to screening carboxylesterase-like genes potentially involved in malathion resistance in oriental migratory locust (Locusta migratoria manilensis). Pest Manag. Sci 2011, 67:183-190.
51. Zhou W.W., Liang Q.M., Xu Y., Gurr G.M., Bao Y.Y., Zhou X.P., et al. Genomic insights into the glutathione S-transferase gene family of two rice planthoppers, Nilaparvata lugens (Stal) and Sogatella furcifera (Horvath) (Hemiptera: Delphacidae). PLoS ONE 2013, 8:e56604.
52. Qin G.H., Jia M., Liu T., Zhang X.Y., Guo Y.P., Zhu K.Y., et al. Characterization and functional analysis of four glutathione S-transferases from the migratory locust, Locusta migratoria. PLoS ONE 2013, 8:e58410.
53. Qin G.H., Jia M., Liu T., Zhang X.Y., Guo Y.P., Zhu K.Y., et al. Heterologous expression and characterization of a sigma glutathione S-transferase involved in carbaryl detoxification from oriental migratory locust, Locusta migratoria manilensis (Meyen). J. Insect Physiol 2012, 58:220-227.
54. M. Soumaila Issa, Molecular characterization and functional analysis of cytochrome P450 genes in the yellow fever mosquito Aedes aegypti (Diptera: Culicidae) (Master's thesis), Kansas State University, 2014.
55. Feyereisen R. Insect P450 enzymes. Annu. Rev. Entomol 1999, 44:507-533.
56. Tang T., Zhao C.Q., Feng X.Y., Liu X.Y., Qiu L.H. Knockdown of several components of cytochrome P450 enzyme systems by RNA interference enhances the susceptibility of Helicoverpa armigera to fenvalerate. Pest Manag. Sci 2012, 68:1501-1511.
57. Zhu F., Sams S., Moural T., Haynes K.F., Potter M.F., Palli S.R. RNA interference of NADPH-cytochrome P450 reductase results in reduced insecticide resistance in the bed bug, Cimex lectularius. PLoS ONE 2012, 7:e31037.
58. Zhu F., Gujar H., Gordon J.R., Haynes K.F., Potter M.F., Palli S.R. Bed bugs evolved unique adaptive strategy to resist pyrethroid insecticides. Sci. Rep 2013, 3:1456.
59. Zhu F., Parthasarathy R., Bai H., Woithe K., Kaussmann M., Nauen R., et al. A brain-specific cytochrome P450 responsible for the majority of deltamethrin resistance in the QTC279 strain of Tribolium castaneum. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:8557-8562.
60. Tompkins L.M., Wallace A.D. Mechanisms of cytochrome P450 induction. J. Biochem. Mol. Toxicol 2007, 21:176-181.
61. Sueyoshi T., Negishi M. Phenobarbital response elements of cytochrome P450 genes and nuclear receptors. Annu. Rev. Pharmacol. Toxicol 2001, 41:123-143.
62. Timsit Y.E., Negishi M. CAR and PXR: the xenobiotic-sensing receptors. Steroids 2007, 72:231-246.
63. Kumar P., Pandit S.S., Baldwin I.T. Tobacco rattle virus vector: a rapid and transient means of silencing Manduca sexta genes by plant mediated RNA interference. PLoS ONE 2012, 7:e31347.
64. Whyard S., Singh A.D., Wong S. Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochem. Mol. Biol 2009, 39:824-832.
65. Trivedi B. Bug silencing: the next generation of pesticides. New Sci 2010, 205:34-37.
66. Turner C.T., Davy M.W., MacDiarmid R.M., Plummer K.M., Birch N.P., Newcomb R.D. RNA interference in the light brown apple moth, Epiphyas postvittana (Walker) induced by double-stranded RNA feeding. Insect Mol. Biol 2006, 15:383-391.
67. Pitino M., Coleman A.D., Maffei M.E., Ridout C.J., Hogenhout S.A. Silencing of aphid genes by dsRNA feeding from plants. PLoS ONE 2011, 6:e25709.
68. Bhatia V., Bhattacharya R., Uniyal P.L., Singh R., Niranjan R.S. Host generated siRNAs attenuate expression of serine protease gene in Myzus persicae. PLoS ONE 2012, 7:e46343.
69. Baum J.A., Bogaert T., Clinton W., Heck G.R., Feldmann P., Ilagan O., et al. Control of coleopteran insect pests through RNA interference. Nat. Biotechnol 2007, 25:1322-1326.
70. Mao Y.B., Tao X.Y., Xue X.Y., Wang L.J., Chen X.Y. Cotton plants expressing CYP6AE14 double-stranded RNA show enhanced resistance to bollworms. Transgenic Res 2011, 20:665-673.
71. Tao X.Y., Xue X.Y., Huang Y.P., Chen X.Y., Mao Y.B. Gossypol-enhanced P450 gene pool contributes to cotton bollworm tolerance to a pyrethroid insecticide. Mol. Ecol 2012, 21:4371-4385.
72. Mao Y.B., Xue X.Y., Tao X.Y., Yang C.Q., Wang L.J., Chen X.Y. Cysteine protease enhances plant-mediated bollworm RNA interference. Plant Mol. Biol 2013, 83:119-129.
73. Xiong Y.H., Zeng H.M., Zhang Y.L., Xu D.W., Qiu D.W. Silencing the HaHR3 gene by transgenic plant-mediated RNAi to disrupt Helicoverpa armigera development. Int. J. Biol. Sci 2013, 9:370-381.
74. Zha W.J., Peng X.X., Chen R.Z., Du B., Zhu L.L., He G.C. Knockdown of midgut genes by dsRNA-transgenic plant-mediated RNA interference in the Hemipteran insect Nilaparvata lugens. PLoS ONE 2011, 6:e20504.
75. Mao J.J., Zeng F.R. Plant-mediated RNAi of a gap gene-enhanced tobacco tolerance against the Myzus persicae. Transgenic Res 2014, 23:145-152.
76. Yu X., Wang G., Huang S., Ma Y., Xia L. Engineering plants for aphid resistance: current status and future perspectives. Theor. Appl. Genet 2014, 127(10):2065-2083.
77. Mutti N.S., Louis J., Pappan L.K., Pappan K., Begum K., Chen M.S., et al. A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:9965-9969.
78. Mutti N.S., Park Y., Reese J.C., Reeck G.R. RNAi knockdown of a salivary transcript leading to lethality in the pea aphid, Acyrthosiphon pisum. J. Insect Sci 2006, 6:1-7.
79. Zhang J.Z., Liu X.J., Zhang J.Q., Li D.Q., Sun Y., Guo Y.P., et al. Silencing of two alternative splicing-derived mRNA variants of chitin synthase 1 gene by RNAi is lethal to the oriental migratory locust, Locusta migratoria manilensis (Meyen). Insect Biochem. Mol. Biol 2010, 40:824-833.
80. Zhang X., Zhang J., Zhu K.Y. 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 2010, 19:683-693.
81. Terenius O., Papanicolaou A., Garbutt J.S., Eleftherianos I., Huvenne H., Kanginakudru S., et al. RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J. Insect Physiol 2011, 57:231-245.
82. Luo Y., Wang X., Wang X., Yu D., Chen B., Kang L. Differential responses of migratory locusts to systemic RNA interference via double-stranded RNA injection and feeding. Insect Mol. Biol 2013, 22:574-583.
83. Miyata K., Ramaseshadri P., Zhang Y.J., Segers G., Bolognesi R., Tomoyasu Y. Establishing an in vivo assay system to identify components involved in environmental RNA interference in the Western corn rootworm. PLoS ONE 2014, 9:e101661.
84. Wynant N., Santos D., Verdonck R., Spit J., Van Wielendaele P., Vanden Broeck J. Identification, functional characterization and phylogenetic analysis of double stranded RNA degrading enzymes present in the gut of the desert locust, Schistocerca gregaria. Insect Biochem. Mol. Biol 2014, 46:1-8.
85. Wang Y.B., Zhang H., Li H.C., Miao X.X. Second-generation sequencing supply an effective way to screen RNAi targets in large scale for potential application in pest insect control. PLoS ONE 2011, 6:e18644.
86. Wang Z., Gerstein M., Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet 2009, 10:57-63.