Feasibility, limitation and possible solutions of RNAi-based technology for insect pest control

Insect Science

Volumn 20, Issue 1, 2013, Pages 15-30

  Zhang, Hao ^a,b   Li, Hai Chao ^a   Miao, Xue Xia ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Delivery; DsRNA; Insect pest control; RNAi; Screen

Indexed keywords

DOUBLE STRANDED RNA; INSECT PROTEIN;

ANIMAL; DELIVERY; DSRNA; GENE TRANSFER; GENETICS; INSECT; INSECT CONTROL; INSECT PEST CONTROL; METABOLISM; METHODOLOGY; REVIEW; RNA INTERFERENCE; RNAI; SCREEN;

DELIVERY; DSRNA; INSECT PEST CONTROL; RNAI; SCREEN;

ANIMALS; GENE TRANSFER TECHNIQUES; INSECT CONTROL; INSECT PROTEINS; INSECTS; RNA INTERFERENCE; RNA, DOUBLE-STRANDED;

HEXAPODA;

EID: 84872792699     PISSN: 16729609     EISSN: 17447917     Source Type: Journal    
DOI: 10.1111/j.1744-7917.2012.01513.x     Document Type: Review

References (92)

1. Alsford, S., Turner, D.J., Obado, S.O., Sanchez-Flores, A., Glover, L., Berriman, M., Hertz-Fowler, C. and Horn, D. (2011) High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Research, 21, 915-924.
2. Araujo, R.N., Santos, A., Pinto, F.S., Gontijo, N.F., Lehane, M.J. and 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 Biochemistry and Molecular Biology, 36, 683-693.
3. Aronstein, K., Pankiw, T. and Saldivar, E. (2006) SID-I is implicated in systemic gene silencing in the honey bee. Journal of Apicultural Research, 45, 20-24.
4. Asmann, Y.W., Klee, E.W., Thompson, E.A., Perez, E.A., Middha, S., Oberg, A.L., Therneau, T.M., Smith, D.I., Poland, G.A., Wieben, E.D. and Kocher, J.P.A. (2009) 3′ tag digital gene expression profiling of human brain and universal reference RNA using Illumina Genome Analyzer. BMC Genomics, 10: 531.
5. Bai, H., Zhu, F., Shah, K. and Palli, S.R. (2011) Large-scale RNAi screen of G protein-coupled receptors involved in larval growth, molting and metamorphosis in the red flour beetle. BMC Genomics, 12: 388.
6. Baum, J.A., Bogaert, T., Clinton, W., Heck, G.R., Feldmann, P., Ilagan, O., Johnson, S., Plaetinck, G., Munyikwa, T., Pleau, M., Vaughn, T. and Roberts, J. (2007) Control of coleopteran insect pests through RNA interference. Nature Biotechnology, 25, 1322-1326.
7. Bautista, Ma.A.M., Miyata, T., Miura, K. and Tanaka, T. (2009) RNA interference-mediated knockdown of a cytochrome P450, CYP6BG1, from the diamondback moth, Plutella xylostella, reduces larval resistance to permethrin. Insect Biochemistry and Molecular Biology, 39, 38-46.
8. Bettencourt, R., Terenius, O. and Faye, I. (2002) Hemolin gene silencing by ds-RNA injected into Cecropia pupae is lethal to next generation embryos. Insect Molecular Biology, 11, 267-271.
9. Bucher, G., Scholten, J. and Klingler, M. (2002) Parental RNAi in Tribolium (Coleoptera). Current Biology, 12, R85-R86.
10. Chen, J., Zhang, D., Yao, Q., Zhang, J., Dong, X., Tian, H., Chen, J. and Zhang, W. (2010) Feeding-based RNA interference of a trehalose phosphate synthase gene in the brown planthopper, Nilaparvata lugens. Insect Molecular Biology, 19, 777-786.
11. Clynen, E., Ciudad, L., Belles, X. and Piulachs, M.D. (2011) Conservation of fruitless' role as master regulator of male courtship behaviour from cockroaches to flies. Development Genes and Evolution, 221, 43-48.
12. Cronin, S.J.F., Nehme, N.T., Limmer, S., Liegeois, S., Pospisilik, J.A., Schramek, D., Leibbrandt, A., Simoes, R.D.M., Gruber, S., Puc, U., Ebersberger, I., Zoranovic, T., Neely, G.G., Haeseler, A.V., Ferrandon, D. and Penninger, J.M. (2009) Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science, 325, 340-342.
13. Dabour, N., Bando, T., Nakamura, T., Miyawaki, K., Mito, T., Ohuchi, H. and Noji, S. (2011) Cricket body size is altered by systemic RNAi against insulin signaling components and epidermal growth factor receptor. Development Growth & Differentiation, 53, 857-869.
14. Dong, Y. and Friedrich, M. (2005) Nymphal RNAi: systemic RNAi mediated gene knockdown in juvenile grasshopper. BMC Biotechnology, 5: 25.
15. Elaine, B.A., Miguel, S.S. and Christopher, R.M. (2005) Mechanisms of hopperburn: An overview of insect taxonomy, behavior, and physiology. Annual Review of Entomology, 50, 125-151.
16. Fire, A., Xu, S., Montgomery, M.K., Kostas, S.A., Driver, S.E. and Mello, C.C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature, 391, 806-811.
17. Fire, A.Z. (2007) Gene silencing by double-stranded RNA (Nobel lecture). Cell Death and Differentiation, 14, 1998-2012.
18. Gan, D., Zhang, J., Jiang, H., Jiang, T., Zhu, S. and Cheng, B. (2010) Bacterially expressed dsRNA protects maize against SCMV infection. Plant Cell Reports, 29, 1261-1268.
19. Gatehouse, J.A. and Price, D.R.G. (2011) Protection of crops against insect pests using RNA interference. Insect Biotechnology, 2, 145-168.
20. Gong, L.A., Yang, X.Q., Zhang, B.L., Zhong, G.H. and Hu, M.Y. (2011) Silencing of Rieske iron-sulfur protein using chemically synthesised siRNA as a potential biopesticide against Plutella xylostella. Pest Management Science, 67, 514-520.
21. Gordon, K.H.J. and Waterhouse, P.M. (2007) RNAi for insect-proof plants. Nature Biotechnology, 25, 1231-1232.
22. Griebler, M., Westerlund, S.A., Hoffmann, K.H. and 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. Journal of Insect Physiology, 54, 997-1007.
23. Yang, G., You, M.S., Vasseur, L., Zhao, Y. and Liu C.H. (2011) Development of RNAi in insects and RNAi-based pest control. Pesticides in the Modern World-Pest Contral and Pesticides Exposure and Toxicity Assessment (ed. M. Stoytcheva ), pp. 28-38. InTech.
24. Guo, S. and Kemph, K.J. (1995) par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell, 81, 611-620.
25. Gvakharia, B.O., Bebas, P., Cymborowski, B. and Giebultowicz, J.M. (2003) Disruption of sperm release from insect testes by cytochalasin and beta-actin mRNA mediated interference. Cellular and Molecular Life Sciences, 60, 1744-1751.
26. Haas, B.J. and Zody, M.C. (2010) Advancing RNA-Seq analysis. Nature Biotechnology, 28, 421-423.
27. Huang, J.H. and Lee, H.J. (2011) RNA interference unveils functions of the hypertrehalosemic hormone on cyclic fluctuation of hemolymph trehalose and oviposition in the virgin female Blattella germanica. Journal of Insect Physiology, 57, 858-864.
28. Huvenne, H. and Smagghe, G. (2010) Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. Journal of Insect Physiology, 56, 227-235.
29. Ikeno, T., Numata, H. and Goto, S.G. (2011a) Circadian clock genes period and cycle regulate photoperiodic diapause in the bean bug Riptortus pedestris males. Journal of Insect Physiology, 57, 935-938.
30. Ikeno, T., Numata, H. and Goto, S.G. (2011b) Photoperiodic response requires mammalian-type cryptochrome in the bean bug Riptortus pedestris. Biochemical and Biophysical Research Communications, 410, 394-397.
31. Irles, P. and Piulachs, M.D. (2011) Citrus, a key insect eggshell protein. Insect Biochemistry and Molecular Biology, 41, 101-108.
32. Jaubert-Possamai, S., Trionnaire, G.Le, Bonhomme, J., Christophides, G.K., Rispe, C. and Tagu, D. (2007) Gene knockdown by RNAi in the pea aphid Acyrthosiphon pisum. BMC Biotechnology, 7: 63.
33. Jose, A.M. and Hunter, C.P. (2007) Transport of sequence-specific RNA interference information between cells. Annual Review of Genetics, 41, 305-330.
34. Khajuria, C., Buschman, L.L., Chen, M.S., Muthukrishnan, S. and Zhu, K.Y. (2010) A gut-specific chitinase gene essential for regulation of chitin content of peritrophic matrix and growth of Ostrinia nubilalis larvae. Insect Biochemistry and Molecular Biology, 40, 621-629.
35. Kiger, A., Baum, B., Jones, S., Jones, M., Coulson, A., Echeverri, C. and Perrimon, N. (2003) A functional genomic analysis of cell morphology using RNA interference. Journal of Biology, 2, 1-15.
36. Kotwica, J., Bebas, P., Gvakharia, B.O. and Giebultowicz, J.M. (2009) RNA interference of the period gene affects the rhythm of sperm release in moths. Journal of Biological Rhythms, 24, 25-34.
37. Kumar, M., Gupta, G.P. and Rajam, M.V. (2009) Silencing of acetylcholinesterase gene of Helicoverpa armigera by siRNA affects larval growth and its life cycle. Journal of Insect Physiology, 55, 273-278.
38. Kurreck, J. (2009) RNA interference: From basic research to therapeutic applications. Angewandte Chemie (International Edition in English), 48, 1378-1398.
39. Lee, C.M., Su, M.T. and Lee, H.J. (2009) Pigment dispersing factor: An output regulator of the circadian clock in the German cockroach. Journal of Biological Rhythms, 24, 35-43.
40. Lee, S., Shrestha, S., Prasad, S.V. and Kim, Y. (2011) Role of a small G protein Ras in cellular immune response of the beet armyworm, Spodoptera exigua. Journal of Insect Physiology, 57, 356-362.
41. Li, J., Chen, Q., Lin, Y., Jiang, T., Wu, G. and Hua, H. (2011a) RNA interference in Nilaparvata lugens (Homoptera: Delphacidae) based on dsRNA ingestion. Pest Management Science, 67, 852-859.
42. Li, X., Zhang, M. and Zhang, H. (2011b) RNA interference of four genes in adult Bactrocera dorsalis by feeding their dsRNAs. PLoS ONE, 6, e17788.
43. Liu, S., Ding, Z., Zhang, C., Yang, B. and Liu, Z. (2010) Gene knockdown by intro-thoracic injection of double-stranded RNA in the brown planthopper, Nilaparvata lugens. Insect Biochemistry and Molecular Biology, 40, 666-671.
44. Mao, Y.B., Cai, W.J., Wang, J.W., Hong, G.J., Tao, X.Y., Wang, L.J., Huang, Y.P. and Chen, X.Y. (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nature Biotechnology, 25, 1307-1313.
45. Mao, Y.B., Tao, X.Y., Xue, X.Y., Wang, L.J. and Chen, X.Y. (2011) Cotton plants expressing CYP6AE14 double-stranded RNA show enhanced resistance to bollworms. Transgenic Research, 20, 665-673.
46. Martin, D., Maestro, O., Cruz, J., Mane-Padros, D. and Belles, X. (2006) RNAi studies reveal a conserved role for RXR in molting in the cockroach Blattella germanica. Journal of Insect Physiology, 52, 410-416.
47. May, R.C. and Plasterk, R.H. (2005) RNA interference spreading in C. elegans. Methods Enzymology, 392, 308-315.
48. Meister, G. and Tuschl, T. (2004) Mechanisms of gene silencing by double-stranded RNA. Nature, 431, 343-349.
49. Meyering-Vos, M. and Muller, A. (2007) RNA interference suggests sulfakinins as satiety effectors in the cricket Gryllus bimaculatus. Journal of Insect Physiology, 53, 840-848.
50. Mito, T., Nakamura, T., Bando, T., Ohuchi, H. and Noji, S. (2011) The advent of RNA interference in Entomology. Entomological Science, 14, 1-8.
51. Moriyama, Y., Sakamoto, T., Karpova, S.G., Matsumoto, A., Noji, S. and Tomioka, K. (2008) RNA interference of the clock gene period disrupts circadian rhythms in the cricket Gryllus bimaculatus. Journal of Biological Rhythms, 23, 308-318.
52. Morrissy, A.S., Morin, R.D., Delaney, A., Zeng, T., Mcdonald, H., Jones, S., Zhao, Y., Hirst, M. and Marra, M.A. (2009) Next-generation tag sequencing for cancer gene expression profiling. Genome Research, 19, 1825-1835.
53. Mutti, N.S., Park, Y., Reese, J.C. and Reeck, G. (2006) RNAi knockdown of a salivary transcript leading to lethality in the pea aphid, Acyrthosiphon pisum. Journal of Insect Science, 6:1-7.
54. Napoli, C., Lemieux, C. and Jorgensen, R. (1990) lntroduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. The Plant Cell, 2, 279-289.
55. Naranjo, S.E. (2011) Impacts of Bt transgenic cotton on integrated pest management. Journal of Agricultural Food Chemostry, 59, 5842-5851.
56. Niu, B.L., Shen, W.F., Liu, Y., Weng, H.B., He, L.H., Mu, J.J., Wu, Z.L., Jiang, P., Tao, Y.Z. and Meng, Z.Q. (2008) Cloning and RNAi-mediated functional characterization of MaLac2 of the pine sawyer, Monochamus alternatus. Insect Molecular Biology, 17, 303-312.
57. Nybakken, K., Vokes, S.A., Lin, T.Y., Mcmahon, A.P. and Perrimon, N. (2005) A genome-wide RNA interference screen in Drosophila melanogaster cells for new components of the Hh signaling pathway. Nature Genetics, 37, 1323-1332.
58. Pitino, M., Coleman, A.D., Maffei, M.E., Ridout, C.J. and Hogenhout, S.A. (2011) Silencing of aphid genes by dsRNA feeding from plants. PLoS ONE, 6, e25709.
59. Porta, H., Jimenez, G., Cordoba, E., Leon, P., Soberon, M. and Bravo, A. (2011) Tobacco plants expressing the Cry1AbMod toxin suppress tolerance to Cry1Ab toxin of Manduca sexta cadherin-silenced larvae. Insect Biochemistry and Molecular Biology, 41, 513-519.
60. Price, D.R. and Gatehouse, J.A. (2008) RNAi-mediated crop protection against insects. Trends Biotechnology, 26, 393-400.
61. Rajagopal, R., Sivakumar, S., Agrawal, N., Malhotra, P. and Bhatnagar, R.K. (2002) Silencing of midgut aminopeptidase N of Spodoptera litura by double-stranded RNA establishes its role as Bacillus thuringiensis toxin receptor. Journal of Biological Chemistry, 277, 46849-46851.
62. Richards, S., Gibbs, R.A., Weinstock, G.M., Brown, S.J., Denell, R., Beeman, R.W., Gibbs, R., Bucher, G., Friedrich, M., Grimmelikhuijzen, C.J.P., Klingler, M., Lorenzen, M.D., Roth, S., Schroder, R., Tautz, D., Zdobnov, E.M., Muzny, D., Attaway, T., Bell, S., Buhay, C.J., Chandrabose, M.N., Chavez, D., Clerk-Blankenburg, K.P., Cree, A., Dao, M., Davis, C., Chacko, J., Dinh, H., Dugan-Rocha, S., Fowler, G., Garner, T.T., Garnes, J., Gnirke, A., Hawes, A., Hernandez, J., Hines, S., Holder, M., Hume, J., Jhangiani, S.N., Joshi, V., Khan, Z.M., Jackson, L., Kovar, C., Kowis, A., Lee, S., Lewis, L.R., Margolis, J., Morgan, M., Nazareth, L.V., Nguyen, N., Okwuonu, G., Parker, D., Ruiz, S.J., Santibanez, J., Savard, J., Scherer, S.E., Schneider, B., Sodergren, E., Vattahil, S., Villasana, D., White, C.S., Wright, R., Park, Y., Lord, J., Oppert, B., Brown, S., Wang, L.J., Savard, J., Liu, Y., Worley, K., Elsik, C.G., Reese, J.T., Elhaik, E., Landan, G., Graur, D., Arensburger, P., Atkinson, P., Beidler, J., Demuth, J.P., Drury, D.W., Du, Y.Z., Fujiwara, H., Maselli, V., Osanai, M., Robertson, H.M., Tu, Z., Wang, J.J., Wang, S.Z., Song, H., Zhang, L., Sodergren, E., Werner, D., Stanke, M., Morgenstern, B., Solovyev, V., Kosarev, P., Brown, G., Chen, H.C., Ermolaeva, O. and Hlavina, W. (2008) The genome of the model beetle and pest Tribolium castaneum. Nature, 452, 949-955.
63. Shakesby, A.J., Wallace, I.S., Isaacs, H.V., Pritchard, J., Roberts, D.M. and Douglas, A.E. (2009) A water-specific aquaporin involved in aphid osmoregulation. Insect Biochemistry and Molecular Biology, 39, 1-10.
64. Shelton, A.M., Zhao, J.Z. and Roush, R.T. (2002) Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annual Review of Entomology, 47, 845-881.
65. Shu, Y.H., Wang, J.W., Lu, K., Zhou, J.L., Zhou, Q. and Zhang, G.R. (2011) The first vitellogenin receptor from a Lepidopteran insect: molecular characterization, expression patterns and RNA interference analysis. Insect Molecular Biology, 20, 61-73.
66. Sumitani, M., Yamamoto, D.S., Lee, J.M. and Hatakeyama, M. (2005) Isolation of white gene orthologue of the sawfly, Athalia rosae (Hymenoptera) and its functional analysis using RNA interference. Insect Biochemistry and Molecular Biology, 35, 231-240.
67. Takahashi, T., Hamada, A., Miyawaki, K., Matsumoto, Y., Mito, T., Noji, S. and Mizunami, M. (2009) Systemic RNA interference for the study of learning and memory in an insect. Journal of Neuroscience Methods, 179, 9-15.
68. 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. and Smagghe, G. (2011) RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. Journal of Insect Physiology, 57, 231-245.
69. Tian, H., Peng, H., Yao, Q., Chen, H., Xie, Q., Tang, B. and 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.
70. Timmons, L. and Fire, A. (1998) Specific interference by ingested dsRNA. Nature, 395, 854-854.
71. Sijen, T., Fleenor, J., Simmer, F., Thijssen, K.L., Parrish, S., Timmons, L., Plasterk, R.H. and Fire, A. (2001) On the role of RNA amplification in dsRNA-triggered gene silencing. Cell, 107, 465-476.
72. Tomoyasu, Y. and Denell, R.E. (2004) Larval RNAi in Tribolium (Coleoptera) for analyzing adult development. Development Genes and Evolution, 214, 575-578.
73. Tomoyasu, Y., Miller, S.C., Tomita, S., Schoppmeier, M., Grossmann, D. and Bucher, G. (2008) Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biology, 9, R10.
74. Trivedi, B. (2010) Bug silencing: the next generation of pesticides. The New Scientist, 205, 34-37.
75. Turchyn, N., Chesebro, J., Hrycaj, S., Couso, J.P. and Popadic, A. (2011) Evolution of nubbin function in hemimetabolous and holometabolous insect appendages. Developmental Biology, 357, 83-95.
76. Turner, C.T., Davy, M.W., Macdiarmid, R.M., Plummer, K.M., Birch, N.P. and Newcomb, R.D. (2006) RNA interference in the light brown apple moth, Epiphyas postvittana (Walker) induced by double-stranded RNA feeding. Insect Molecular Biology, 15, 383-391.
77. Upadhyay, S.K., Chandrashekar, K., Thakur, N., Verma, P.C., Borgio, J.F., Singh, P.K. and Tuli, R. (2011) RNA interference for the control of whiteflies (Bemisia tabaci) by oral route. Journal of Biosciences, 36, 153-161.
78. Walker, W.B. and Allen, M.L. (2010) Expression and RNA interference of salivary polygalacturonase genes in the tarnished plant bug, Lygus lineolaris. Journal of Insect Science, 10, 1-13.
79. Walker, W.B. and Allen, M.L. (2011) RNA interference-mediated knockdown of IAP in Lygus lineolaris induces mortality in adult and pre-adult life stages. Entomologia Experimentalis et Applicata, 138, 83-92.
80. Walshe, D.P., Lehane, S.M., Lehane, M.J. and Haines, L.R. (2009) Prolonged gene knockdown in the tsetse fly Glossina by feeding double stranded RNA. Insect Molecular Biology, 18, 11-19.
81. Wang, P. and Granados, R.R. (2001) Molecular structure of the peritrophic membrane (PM): identification of potential PM target sites for insect control. Archive of Insect Biochemistry and Physiology, 47, 110-118.
82. Wang, Y.B., Zhang, H., Li, H.C. and Miao, X.X. (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(4), e18644.
83. Wang, Z., Gerstein, M. and Snyder, M. (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nature Reviews Genetics, 10, 57-63.
84. Whyard, S., Singh, A.D. and Wong, S. (2009) Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochemistry and Molecular Biology, 39, 824-832.
85. Winston, W.M., Molodowitch, C. and Hunter, C.P. (2002) Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science, 295, 2456-2459.
86. Wuriyanghan, H., Rosa, C. and Falk, B.W. (2011) Oral delivery of double-stranded RNAs and siRNAs induces RNAi effects in the potato/tomato psyllid, Bactericerca cockerelli. PLoS ONE, 6 (11), e27736.
87. Xu, W.N. and Han, Z.J. (2008) Cloning and phylogenetic analysis of sid-1-like genes from aphids. Journal of Insect Science, 8.
88. Zha, W.J., Peng, X.X., Chen, R.Z., Du, B., Zhu, L.L. and He, G.C. (2011) Knockdown of midgut genes by dsRNA-transgenic plant-mediated RNA interference in the Hemipteran insect Nilaparvata lugens. PLoS ONE, 6(5), e20504.
89. Zhao, Y.Y., Liu, F., Yang, G. and You, M.S. (2011) PsOr1, a potential target for RNA interference-based pest management. Insect Molecular Biology, 20, 97-104.
90. Zhao, Y.Y., Yang, G., Wang-Pruski, G. and You, M.S. (2008) Phyllotreta striolata (Coleoptera: Chrysomelidae): Arginine kinase cloning and RNAi-based pest control. European Journal of Entomology, 105, 815-822.
91. Zhou, X.G., Wheeler, M.M., Oi, F.M. and Scharf, M.E. (2008) RNA interference in the termite Reticulitermes flavipes through ingestion of double-stranded RNA. Insect Biochemistry and Molecular Biology, 38, 805-815.
92. Zhu, F., Xu, J.J., Palli, R., Ferguson, J. and Palli, S.R. (2011) Ingested RNA interference for managing the populations of the Colorado potato beetle, Leptinotarsa decemlineata. Pest Management Science, 67, 175-182.