Key enzymes and proteins of crop insects as candidate for RNAi based gene silencing

Frontiers in Physiology

Volumn 6, Issue MAR, 2015, Pages

  Vijaya Sudhakara Rao, K ^a   Renuka, P ^a   Sheshu Madhav, M ^a   Mangrauthia, Satendra K ^a  

^a DIRECTORATE OF RICE RESEARCH   (India)

Author keywords

Dicer; Insecticide; Off target; Resistance; siRNA

Indexed keywords

ACETYLCHOLINESTERASE; ALLATOSTATIN; ALLATOTROPIN; ARGININE KINASE; CATALASE; CHITIN SYNTHASE; CYTOCHROME P450; DOUBLE STRANDED RNA; GLUTATHIONE TRANSFERASE; HORMONE RECEPTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; INSECT PROTEIN; INSECTICIDE; MICROSOMAL AMINOPEPTIDASE; REGULATOR PROTEIN; RNA INDUCED SILENCING COMPLEX; SMALL INTERFERING RNA; STRUCTURAL PROTEIN; TRYPTOPHAN 2,3 DIOXYGENASE; VITELLOGENIN;

ARTICLE; CAENORHABDITIS ELEGANS; CROP PROTECTION; DROSOPHILA MELANOGASTER; GENE SEQUENCE; GENE SILENCING; GENE TARGETING; HELICOVERPA ARMIGERA; INSECT CONTROL; INSECT GENOME; INSECT RESISTANCE; INSECTICIDE RESISTANCE; NONHUMAN; PEST INSECT; RNA INTERFERENCE; SEQUENCE DATABASE; TRANSGENE; TRANSGENIC PLANT;

EID: 84926473226     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2015.00119     Document Type: Article

References (158)

1. Abdel-latief, M.A., and Hoffmann, K. H. (2014). Functional activity of allatotropin and allatostatin in the pupal stage of a holometablous insect, Tribolium castaneum (Coleoptera, Tenebrionidae). Peptides 53, 172-184. doi: 10.1016/j.peptides.2013.10.007.
2. Adams, M.D., Celniker, S.E., Holt, R.A., Evans, C.A., Gocayne, J.D., Amanatides, P.G., et al. (2000). The genome sequence of Drosophila melanogaster. Science 287, 2185-2195.
3. Agarwal, S., and Mangrauthia, S. K. (2013). Advances, challenges and prospects in Small RNA Mediated approaches of Virus Resistance in Plants. Journal of Genomes and Exomes2, 43-62. doi: 10.4137/JGE.S11938.
4. Agarwal, S., Mohan, M., and Mangrauthia, S. K. (2012). RNAi: Machinery and role in pest and disease management. In Crop stress and its management: perspectives and strategies. Springer Netherlands, pp 447-469. DOI 10.1007/978-94-007-2220-0_13
5. Ai, T., Zhang, L., Gao, Z., Zhu, C. X., and Guo, X. (2011). Highly efficient virus resistance mediated by artificial microRNAs that target the suppressor of PVX and PVY in plants. Plant Biol (Stuttg).13, 304-316. doi: 10.1111/j.1438-8677.2010.00374.x.
6. Alves, A.P., Lorenzen, M. D., Beeman, R. W., Foster, J. E., and Siegfried, B. D.(2010). RNA interference as a method for target-site screening in the Western corn rootworm, Diabrotica virgifera virgifera. J Insect Sci. 10, 1-16. doi: 10.1673/031.010.14122.
7. Amdam, G.V., Simoes, Z.L., Guidugli, K.R., Norberg, K., and Omholt, S.W. (2003). Disruption of vitellogenin gene function in adult honeybees by intra-abdominal injection of double-stranded RNA. BMC Biotechnol. 3, 1.
8. Arakane, Y., Muthukrishnan, S., Kramer, K. J., Specht, C. A., Tomoyasu, Y., Lorenzen, M. D., et al. (2005). The Tribolium chitin synthase genes TcCHS1 and TcCHS2 are specialized for synthesis of epidermal cuticle and midgut peritrophic matrix. Insect Mol. Biol.14, 453-463.
9. Arakane, Y., and Muthukrishnan, S. (2010). Insect chitinase and chitinase-like proteins. Cell Mol Life Sci. 67, 201-216. doi: 10.1007/s00018-009-0161-9.
10. 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 Biochem Mol Biol. 36, 683-93. doi:10.1016/j.ibmb.2006.05.012.
11. Ashida, M., Reiko, I., and Yoshida, H. (1982). Control and function of the prophenoloxidase activating system.In:Proc.3rd Int.Collog. Invertebrate pathonogy, University of Sussex, Brighton, pp.81-86.
12. Attardo, G. M., Guz, N., Strickler-Dinglasan, P., and Aksoy, S. (2006). Molecular aspects of viviparous reproductive biology of the tsetse fly (Glossina morsitans morsitans): regulation of yolk and milk gland protein synthesis. J Insect Physiol. 52, 1128-36. doi: 10.1016/j.jinsphys.2006.07.007.
13. Ayme-Southgate, A. J., Turner, L., and Southgate, R. J. (2013).Molecular analysis of the muscle protein projectin in Lepidoptera. J Insect Sci. 13. doi: 10.1673/031.013.8801.
14. Balczun, C., Siemanowski, J., Pausch, J. K., Helling, S., Marcus, K., Stephan, C., et al. (2012) Intestinal aspartate proteases TiCatD and TiCatD2 of the haematophagous bug Triatoma infestans Reduviidae): sequence characterisation, expression pattern and characterisation of proteolytic activity. Insect Biochem Mol Biol. 42, 240-50. doi: 10.1016/j.ibmb.2011.12.006.
15. Baum, J. A., Bogaert, T., Clinton, W., Heck, G. R., Feldmann, P., Ilagan, O., et al.(2007). Control of coleopteran insect pests through RNA interference. Nat Biotechnol. 25, 1322-1326. doi:10.1038/nbt1359.
16. Bautista, M. A., 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 Biochem Mol Biol. 39, 38-46. doi: 10.1016/j.ibmb.2008.09.005.
17. Beckage, N. E. (2000). Insect growth regulators. Biological and Biotechnological Control of Insect Pests ed. J. E. Rechcigl, N.A. Rechcigl. (Lewis Publishers, Boca Raton, London, NewYork, Washington, D.C). 123-137.
18. Beverley, S. M., and Wilson, A. C. (1982). Molecular evolution in Drosophila and higher dipteral. J Mol Evol. 18, 251-264. doi:10.1007/BF01734103.
19. Bown, D. P., and Gatehouse, J. A. (2004). Characterization of a digestive carboxypeptidase from the insect pest corn earworm (Helicoverpa armigera) with novel specificity towards C-terminal glutamate residues. Eur J Biochem. 271. 2000-2011. doi: 10.1111/j.1432-1033.2004.04113.x.
20. Bragatto, I., Genta, F. A., Ribeiro, A. F., Terra, W. R., and Ferreira, C. (2010). Characterization of a ß-1, 3-glucanase active in the alkaline midgut of Spodoptera frugiperda larvae and its relation to ß- glucan-binding proteins. Insect Biochem Mol Biol. 40, 861-872. doi: 10.1016/j.ibmb.2010.08.006.
21. Brennan, Y., Callen, W. N., Christoffersen, L., Dupree, P., Goubet, F., Healey, S., et al. (2004). Unusual microbial xylanases from insect guts. Appl Environ Microbiol. 70, 3609-3617.
22. Brown, A.E., and Ingianni, E. (2013). Mode of Action of Insecticides and Related Pest Control Chemicals for Production Agriculture, Ornamentals, and Turf, Pesticide information Leaf let. University of Maryland Pesticide Education and Assessment Programs.1-13. http://pesticide/umd.edu.
23. Brown, S.J., Mahaffey, J.P., Lorenzen, M.D., Denell, R.E. and Mahaffey J.W. (1999). Using RNAi to investigate orthologous homeotic gene function during development of distantly related insects. Evol Dev. 1, 11-15.
24. Bucher, G., Scholten, J., and Klingler, M. (2002). Parental RNAi in Tribolium (Coleoptera). Curr Biol.12, R85-R86.
25. Chapman, R. F. (1998).The Insects: Structure and Function. 4th edition. Online. ISBN: 9780511818202, Hardback ISBN:9780521570480, Paperback ISBN:9780521578905. Cambridge University Press.
26. Chen, J., Zhang, D., Yao, Q., Zhang, J., Dong, X., Tian, H., et al. (2010). Feeding-based RNA interference of a trehalose phosphate synthase gene in the brown planthopper, Nilaparvata lugens. Insect Mol Biol. 19, 777-786. doi: 10.1111/j.1365-2583.2010.01038.x.
27. Chen, R. P., Liu, C. Y., Shao, H. L., Zheng, W. W., Wang, J. X., and Zhao, X. F. (2012). Adenylate kinase 2 (AK2) promotes cell proliferation in insect development. BMC Mol Biol. 13. doi: 10.1186/1471-2199-13-31.
28. Chen, X., Lu, S., and Zhang, Y. (2014). Characterization of Protein Phosphatase 5 from Three Lepidopteran Insects: Helicoverpa armigera, Mythimna separata and Plutella xylostella. PLoS One. 9:e97437. doi:10.1371/journal.pone.0097437.
29. Chen, X., Tian, H., Zou, L., Tang, B., Hu, J., and Zhang, W. (2008). Disruption of Spodoptera exigua larval development by silencing chitin synthase gene A with RNA interference. Bull Entomol Res. 98, 613-619. doi: 10.1017/S0007485308005932.
30. Chirila, T. V., Suzuki, S., Bray, L. J., Barnett, N. L., and Harkin, D. G. (2013). Evaluation of silk sericin as a biomaterial: in vitro growth of human corneal limbal epithelial cells on Bombyx mori sericin membranes. Progress in Biomaterials 2, 1-10.
31. Christeller, J. T., Markwick, N. P., and Burgess, E. P. J. (1994). Midgut proteinase activities of three keratinolytic larvae, Hofmannophila pseudospretella, Tineola bisselliella, and Anthrenocerus australis, and the effect of proteinase inhibitors on proteolysis. Arch Insect Biochem Physiol 25, 159- 173. doi: 10.1002/arch.940250207.
32. Coleman, A.D., Wouters, R.H.M., Mugford, S.T., and Hogenhout, S.A. (2014). Persistence and transgenerational effect of plant-mediated RNAi in aphids. J Exp Bot. doi: 10.1093/jxb/eru450.
33. Crabtree, B., Higgins, S. J., and Newsholme, E. A. (1972). The activities of pyruvate carboxylase, phosphoenolpyruvate carboxylase and fructose diphosphatase in muscles from vertebrates and invertebrates. Biochem J. 130, 391-396.
34. Cruz, J., Mane-Padros, D., Belles, X., and Martin, D. (2006). Functions of the ecdysone receptor isoform-A in the hemimetabolous insect Blattella germanica revealed by systemic RNAi in vivo. Dev Biol. 297, 158-171.
35. Csikos, G., Molnar, K., Borhegyi, N. H., Talian, G. C., and Sass, M. (1999). Insect cuticle, an in vivo model of protein trafficking. J Cell Sci.112, 2113-2124.
36. Dong, Y., and Friedrich, M. (2005). Nymphal RNAi: systemic RNAi mediated gene knockdown in juvenile grasshopper. BMC Biotechnol. 3, 5-25.doi:10.1186/1472-6750-5-25.
37. Duan, C. G., Wang, C. H., and Guo, H. S. (2012). Application of RNA silencing to plant disease resistance. Silence 3, 1-8. doi: 10.1186/1758-907X-3-5.
38. Emmons, R. B., Duncan, D., Estes, P. A., Kiefel, P., Mosher, J. T., Sonnenfeld, M., et al. (1999). The spineless-aristapedia and tango bHLH-PAS proteins interact to control antennal and tarsal development in Drosophila. Development 126, 3937-3945.
39. Fellmann, C., and Lowe, S. W. (2014). Stable RNA interference rules for silencing, Nat. Cell Biol.16,10-18.doi:10.1038/ncb2895.
40. Ferguson, C., Lakey, A., Hutchings, A., Butcher, G.W., Leonard, K.R., and Bullard, B. (1994). Cytoskeletal proteins of insect muscle: location of zeelins in Lethocerus flight and leg muscle. J Cell Sci. 107, 1115-1129.
41. Feyereisen, R. (1999). Insect P450 enzymes. Annu Rev Entomol. 44, 507-533.
42. Firmino A.A.P., Fonseca, F.C.dA., de Macedo, L.L.P., Coelho, R. R., Antonino de Souza Jr, J. D. (2013).Transcriptome Analysis in Cotton Boll Weevil (Anthonomus grandis) and RNA Interference in Insect Pests. PLoS ONE. 8. doi:10.1371/journal.pone.0085079.
43. Fischer, R., Ostafe, R., and Twyman, R. M. (2013). Cellulases from Insects. Adv Biochem Eng Biotechnol. 136, 51-64. doi:10.1007/10_2013_206.
44. Fraga, A., Ribeiro, L., Lobato, M., Santos, V., and Silva, J. R. (2013). Glycogen and Glucose Metabolism Are Essential for Early Embryonic Development of the Red Flour Beetle Tribolium castaneum. PLoS One. 8: e65125. doi:10.1371/journal.pone.0065125.
45. Gatehouse, J.A., and Price D.R.G. (2011). Protection of Crops Against Insect Pests Using RNA Interference. In: Vilcinskas, A. (ed.) Insect Biotechnology. Springer publications.145-168.
46. Giannopoulos, N. G., Michalopoulos, I., Papandreou, N. C., Malatras, A., Iconomidou, V. A., and Hamodrakas, S. J. (2013). LepChorion.DB, a database of Lepidopteran chorion proteins and a set of tools useful for the identification of chorion proteins in Lepidopteran proteomes. Insect Biochem Mol Biol. 43, 189-196. doi: 10.1016/j.ibmb.2012.12.001.
47. Gorbacheva, T. M., Syromyatnicov, M. Yu., Popov, V. N., Lopatin, A. V., Eprintsev, A. T., and Fedorin, D. N. (2013). Characteristics of functioning of succinate dehydrogenase from flight muscles of the bumblebee Bombus terrestris (L.) Akademii Nauk, Seriya Biologicheskaya.(Izvestiya).40, 429- 434. doi: 10.1134/S1062359013050051.
48. Gordon, K. H .J., and Waterhouse, P. M. (2007). RNAi for insect-proof plants. Nat Biotechnol. 25, 1231-1232. doi:10.1038/nbt1107-1231.
49. Gui, Z. Z., Lee, K. S., Kim, B. Y., Choi, Y. S., Wei, Y. D., Choo, Y. M., et al. (2006). Functional role of aspartic proteinase cathepsin D in insect Metamorphosis, BMC Dev Biol. 6:49. doi:10.1186/1471-213X-6-49.
50. Gullan, P. J., and Cranston, P. S. (2010). The Insects: An Outline of Entomology. Wiley-Blackwell. www.wiley.com/go/gullan/insects.
51. Gvakharia, B. O., Bebas, P., Cymborowski, B., Giebultowicz, J. M. (2003). Disruption of sperm release from insect testes by cytochalasin and beta-actin mRNA mediated interference. Cell Mol. Life Sci. 60, 1744-1751.
52. Hammond, S.M., Bernstein, E., Beach, D. and Havvon, G. J. (2000). An RNA directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature. 404: 293-296.
53. Healy, J. A., Cross, T. F., and Healy, A. (2004). The alpha-Gpdh polymorphism in the tick Ixodes ricinus: similar diurnal trends in genotypic composition in Irish and Swedish population samples. Exp Appl Acarol. 32(1-2):111-8.
54. Hensbergen, P.J., van Velzen, M. J., Nugroho, R. A., Donker, M. H., and van Straalen, N. M. (2000). Metallothionein-bound cadmium in the gut of the insect Orchesella cincta (Collembola) in relation to dietary cadmium exposure. Comp Biochem Physiol C Toxicol Pharmacol. 125, 17-24. doi: 10.1016/S0742-8413(99)00087-0.
55. Hess, C. R., McGuirl, M. M., and Klinman, J. P. (2008). Mechanism of the Insect Enzyme, Tyramine beta Monooxygenase, Reveals Differences from the Mammalian Enzyme, Dopamine beta Monooxygenase. J Biol Che. 283, 3042-3049. doi:10.1074/jbc.M705911200.
56. Hetz, S. K., and Bradley, T. J. (2005). Insects breathe discontinuously to avoid oxygen toxicity. Nature. 433, 516-519. doi:10.1038/nature03106.
57. Hoffmann, K. H, and Lorenz, M. W. (1998). Recent advances in hormones in insect pest control. Phytoparasitica, 26, 323-330. doi:10.1007/BF02981447.
58. Hong-Hua, S.U., Gui-Rong,W., Yong-Jun, Z., Ge-Mei, L., Kong-Ming, W.U., Yu-Yuan, G.(2010). Screening of proteins interacting with Gqa by yeast two-hybrid technique in the antenna of Helicoverpa armigera (Lepidoptera: Noctuidae). Acta Entomol. Sinica , 53, 1339-1344.
59. Huang, Q., Deveraux, Q. L., Maeda, S., Salvesen, G. S., Stennicke, H. R., Hammock, B. D., et al. (2000). Evolutionary conservation of apoptosis mechanisms: Lepidopteran and baculoviral inhibitor of apoptosis proteins are inhibitors of mammalian caspase-9. Proc Natl Acad Sci. 97, 1427-1432.
60. Huvenne, H., and Smagghe, G. (2010). Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J Insect Physiol, 56:227-235.
61. i5K Consortium. (2013). The i5K Initiative: Advancing Arthropod Genomics for Knowledge, Human Health, Agriculture, and the Environment. J Hered,104: 595-600.
62. Insecticide Resistance Action Committee. (2014). Mode of Action Classification Scheme v 7.3. www.irac-online.org/ mode of action team/updated MoA-classification.pdf .
63. Isaac, R. E, Ekbote, U., Coates, D., and Shirras, A.D. (1999).Insect angiotensin-converting enzyme. A processing enzyme with broad substrate specificity and a role in reproduction. Ann N Y Acad Sci. 897, 342-347.
64. Jackson, A. L., Bartz, S. R., Schelter, J., Kobayashi, S.V., Burchard, J., Mao, M., et al. (2003). Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol. 21, 635- 637.doi:10.1038/nbt831.
65. Johnson, N. F., and Triplehorn, C. A. (2005). Borror and DeLong's introduction to the study of insects. (7th ed) Australia: Thomson, Brooks/Cole. ISBN 9780030968358.
66. Kennerdell, J.R., and 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.
67. Kitto, G. B., and Briggs, M. H. (1962). Lactate Dehydrogenase in Some Insect Muscles. Nature. 193, 1003 - 1004. doi:10.1038/1931003b0.
68. Koiwa, H., Shade, R. E., Zhu-Salzman, K., D'Urzo, M. P., Murdock, L.L., Bressan, R. A., et al. (2000). A plant defensive cystatin (soyacystatin) targets cathepsin L-like digestive cysteine proteinases (DvCALs) in the larval midgut of western corn rootworm (Diabrotica virgifera virgifera). FEBS Lett. 471, 67-70. doi: 10.1016/S0014-5793(00)01368-5.
69. 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. J Biol Rhythms. 24, 25-34. doi: 10.1177/0748730408329109.
70. Koch, A., and Kogel, K.H. (2014). New wind in the sails: improving the agronomic value of crop plants through RNAi-mediated gene silencing. Plant Biotechnol J. doi: 10.1111/pbi.12226.
71. Kumar, P., Pandit, S. S., Steppuhn, A., and Baldwin, I. T. (2014). Natural history-driven, plantmediated RNAi-based study reveals CYP6B46's role in a nicotine-mediated antipredator herbivore defense. Proc Natl Acad Sci. 111, 1245-1252. doi: 10.1073/pnas.1314848111.
72. 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. J Insect Physiol. 55 (2009) 273-278. doi: 10.1016/j.jinsphys.2008.12.005.
73. Lecroise, Y.A., Boulard, C., and Keil, B. (1979). Chemical and Enzymatic Characterization of the Collagenase from the Insect. Hypoderma lineatur Eur J Biochem. 101, 385-393.
74. Lemoine, A., Millot, C., Curie, G., Massonneau, V., Delachambre, J. (1993). Monoclonal antibodies recognizing larval- and pupal-specific cuticular proteins of Tenebrio molitor (Insecta, Coleoptera). Roux's Arch Deve Bio. 203, 92-99.
75. Lehane, M., and Billingsley, P. (1996). Biology of the Insect Midgut. Springer Netherlands. doi10.1007/978-94-009-1519-0
76. Liu, S., Zhang, Y. R., Zhou, W.W., Liang, Q. M., Yuan, X., Cheng, J., et al. (2013). Identification and characterization of two sensory neuron membrane proteins from Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). Arch Insect Biochem Physiol. 82, 29-42. doi: 10.1002/arch.21069.
77. Liu, X., Li, J., Guo, W., Li, R., Zhao, D., and Li X. (2014). A New Type I Peritrophic Membrane Protein from Larval Holotrichia oblita (Coleoptera: Melolonthidae) Binds to Chitin. Int J Mol Sci. 15, 6831-6842. doi:10.3390/ijms15046831.
78. Lorenzen, M. D., Brown, S. J., Denell, R. E., and Beeman, R. W. (2002). Cloning and Characterization of the Tribolium castaneum Eye-Color Genes Encoding Tryptophan Oxygenase and Kynurenine 3-Monooxygenase. Genetics. 160, 225-234.
79. Lu, M.X., Liu, Z. X., Cui, Y.D., and Du,Y.Z . (2014). Expression Patterns of Three Heat Shock Proteins in Chilo suppressalis (Lepidoptera: Pyralidae). Ann Entomol Soc Am.107, 667-673. doi: http://dx.doi.org/10.1603/AN13092.
80. Lucas, W. J., Yoo, B. C., and Kragler, F. (2001). RNA as a longdistance information macromolecule in plants. Nat Rev Mol Cell Biol. 2, 849-857. doi:10.1038/35099096.
81. Lungchukiet, P., Donly, B. C., Zhang, J., Tobe, S.S., and Bendena, W.G. (2008). Molecular cloning and characterization of an allatostatin-like receptor in the cockroach Diploptera punctata. Peptides 29, 276-285. doi: 10.1016/j.peptides.2007.10.029.
82. Lynch, J.A., and Desplan, C. (2006). A method for parental RNA interference in the wasp Nasonia vitripennis. Nat Protoc., 1, 486-494.
83. Maeda, I., Kohara, Y., Yamamoto, M., and Sugimoto, A. (2001). Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNA. Curr Biol. 11, 171-176.
84. Mangrauthia, S.K., Singh, P., and Praveen, S. (2010). Genomics of helper component proteinase reveals effective strategy for Papaya ringspot virus resistance. Mol Biotechnol. 44, 22-29. doi: 10.1007/s12033-009-9205-5.
85. Mao, Y. B., Cai, W. J., Wang, J. W., Hong, G. J., Tao, X. Y., Wang, L. J., et al.(2007). Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat Biotechnol. 25, 1307-13.
86. McGavin, G.C. (2001). Essential Entomology: An Order-by-Order Introduction. Oxford: Oxford University Press. ISBN 9780198500025.
87. Misquitta, L., and Paterson, B.M.(1999). Targeted disruption of gene function in Drosophila by RNA interference (RNA-i): A role for nautilus in embryonic somatic muscle formation. Proc Natl Acad Sci USA. 96, 1451-1456.
88. 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. J Biol Rhythms.23, 308-318. doi: 10.1177/0748730408320486.
89. Mutti, N.S., Park, Y., Reese, J.C., and Reeck, G.R. (2006). RNAi Knockdown of a Salivary Transcript Leading to Lethality in the Pea Aphid, Acyrthosiphon pisum. J Insect Sci. 6, 1-7. DOI: 10.1673/031.006.3801.
90. Nakayashiki, H., and Nguyen, Q. B. (2008). RNA interference: roles in fungal biology. Curr Opin Microbiol. 11, 494-502.doi: 10.1016/j.mib.2008.10.001.
91. Nauen, R., and Denholm, I. (2005). Resistance of Insect Pests to Neonicotinoid Insecticides:Current Status and Future Prospects. Arch Insect Biochem Physiol. 58:200-215.doi: 10.1002/arch.20043.
92. Nauen, R., and Bretschneider, T.(2002). New modes of action of insecticides. Pesticide Outlook 13, 241-245.doi: 10.1039/B211171N.
93. Neuman-Silberberg, F. S., and Schüpbach, T. (1996). The Drosophila TGF-alpha-like protein Gurken: expression and cellular localization during Drosophila oogenesis. Mech Dev. 59,105-113. DOI: 10.1016/0925-4773(96)00567-9.
94. Odman-Naresh, J., Duevel, M., Muthukrishnan, S., and Merzendorfer, H. (2013). A Lepidopteran- Specific Gene Family Encoding Valine-Rich Midgut Proteins. PLoSONE 8: e82015. doi:10.1371/journal.pone.0082015.
95. Pitino, M., Coleman, A., Maffei, M., Ridout, C., and Hogenhout, S. (2011). Silencing of aphid genes by dsRNA feeding from plants. PLoSONE 6: e25709.
96. Praveen, S., and Mangrauthia, S. K. (2006). Viral suppressors: small RNA regulators. Indian J Virol. 17, 67-77.
97. Price, D. R. G., and Gatehouse, J. A. (2008). RNAi mediated crop protection against insects. Trends Biotechnol. 26, 393-400. doi: 10.1016/j.tibtech.
98. 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. J Biol Chem. 277,46849-46851.
99. Reiko,I., and Ashida, M. (1986). Biosynthesis of prophenoloxidase in hemocytes of larval hemolymph of the silkworms, Bombyx mori. Insect Biochem. 16, 547-555.
100. Rogers, M. E., Krieger, J., and Vogt, R. G. (2001). Antennal SNMPs (sensory neuron membrane proteins) of Lepidoptera define a unique family of invertebrate CD36-like proteins. J Neurobiology. 49, 47-61. doi: 10.1002/neu.1065.
101. Ruiz-Medrano, R., Xoconostle-Cázares, B., Lucas, W. J.(1999). Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. Development126.4405-4419.
102. Schoofs, L., Clynen, E., and Salzet, M. (2002). Trypsin and Chymotrypsin Inhibitors in Insects and Gut Leeches. Curr Pharm Des. 8,483-491.doi: 10.2174/1381612023395718.
103. Schwab, R., Ossowski, S., Riester, M., Warthmann, N., and Weigel, D.(2006). Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18, 1121- 1133.doi:10.1105/tpc.105.039834.
104. Scott, J.G., Michel, K., Bartholomay, L.C., Siegfried, B. D., Hunter, W. B., Smagghe, G., et al. (2013). Towards the elements of successful insect RNAi. J Insect Physiol. 59, 1212-1221. doi: 10.1016/j.jinsphys.2013.08.014.
105. Senthil-Kumar, M., and Mysore, K.S. (2011). Caveat of RNAi in Plants: The Off-Target Effect. In: H. Kodama, A. Komamine (eds.), RNAi and Plant Gene Function Analysis, Methods in Molecular Biology 744, DOI 10.1007/978-1-61779-123-9_2, Springer Science+Business Media1
106. Shabalina, S.A., and Koonin., E.V.( 2008). Origins and evolution of eukaryotic RNA interference. Trends Ecol Evol. 23, 578-587. doi: 10.1016/j.tree.2008.06.005.
107. Shappirio, D.G. (1974). Comparative studies of oxidative enzyme systems in epidermis and fat body of diapausing and non-diapausing silkmoths. J Insect Physiol. 20, 291- 300.
108. Shinoda, T., and Itoyama, K. (2003). Juvenile hormone acid methyltransferase: A key regulatory enzyme for insect metamorphosis. Proc Natl Acad Sci USA. 100, 11986-11991. doi:10.1073/pnas.2134232100.
109. 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 Mol Biol. 20, 61-73. doi: 10.1111/j.1365-2583.2010.01054.x.
110. Sim, C., and Denlinger, D. L. (2011). Catalase and superoxide dismutase-2 enhance survival and protect ovaries during overwintering diapause in the mosquito Culex pipiens. J Insect Physiol. 57, 628-34. doi: 10.1016/j.jinsphys.2011.01.012.
111. Sivakumar, S., Rajagopal, R., Venkatesh, G. R., Srivastava, A., and 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.
112. Sparagana, S. P., Bhaskaran, G., and Barrera, P. (1985). Juvenile hormone acid methyltransferase activity in imaginal discs of Manduca sexta prepupae. Arch Insect Biochem Physiol. 2, 191- 202.doi: 10.1002/arch.940020207.
113. Spring, J. H., Robichaux, S. R., and Hamlin, J. A. (2009). The role of aquaporins in excretion in insects. J Exp Biol. 212, 358-362. doi: 10.1242/jeb.024794.
114. Steele, J. E. (1982). Glycogen phosphorylase in insects. Insect Biochem. 12, 131 -147. DOI: 10.1016/0020-1790(82)90001-4.
115. Strickler-Dinglasan, P. M., Guz, N., Attardo, G., and Aksoy, S. (2006). Molecular characterization of iron binding proteins from Glossina morsitans morsitans (Diptera: Glossinidae). Insect Biochem Mol Biol. 36, 921-933.doi: 10.1016/j.ibmb.2006.09.003.
116. Suiter, D. R., and Scharf, M. E. (2011). Insecticide Basics for the Pest Management Professional. University of Georgia Bulletin. 1352, 1-24.
117. Suzuki, Y., Truman, J.W., and Riddiford, L.M. (2008). The role of Broad in the development of Tribolium castaneum: implications for the evolution of the holometabolous insect pupa. Development 135, 569-577. doi: 10.1242/dev.015263.
118. Swingle, H. S. (1925). The Ohio Journal of Science. 25, 209-218, http://hdl.handle.net/1811/2281.
119. Tabara, H., Grishok, A., and Mello, C.C. (1998). RNAi in C. elegans: soaking in the genome sequence. Science 282, 430-431.
120. Tang, B., Wang, S., and Zhang, F. (2010). Two storage hexamerins from the beet armyworm Spodoptera exigua: Cloning, characterization and the effect of gene silencing on survival. BMC Mol Biol 11. doi:10.1186/1471-2199-11-65.
121. Tang, B., Xu, Q., Zou, Q., Fang, Q., Wang, S., and Ye, G. (2012). Sequencing and characterization of glycogen synthase and glycogen phosphorylase genes from Spodoptera exigua and analysis of their function in starvation and excessive sugar intake. Arch Insect Biochem Physiol. 80, 42-62. doi: 10.1002/arch.21027.
122. Thakur, N., Upadhyay, S., Verma, P., Chandrashekar, K., Tuli, R., and Singh, P.K. (2014). Enhanced Whitefly Resistance in Transgenic Tobacco Plants Expressing Double Stranded RNA of v-ATPaseA Gene. PLOS One. 9, e87235.
123. Thany, S. H., Leignel, T. H., and Lapied, B. (2010). Identification of cholinergic synaptic transmission in the insect nervous system. Adv Exp Med Biol. 683, 1-10.
124. Timmons, L., and Fire, A. (1998). Specific interference by ingested dsRNA. Nature. 395(6705), 854.
125. Tomari, Y., and Zamore, P.O. (2005). Perspective: Machines for RNAi. Genes Dev. 19, 517-529.
126. 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 Biol. 9, R10 (doi:10.1186/gb-2008-9-1-r10).
127. 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 Mol Biol. 15, 383-91. doi: 10.1111/j.1365-2583.2006.00656.x
128. Upadhyay, S. K., Chandrashekar, K., Thakur, N., Verma, P. C., Borgio, J.F., Singh, P. K., et al. (2011). RNA interference for the control of whiteflies (Bemisia tabaci) by oral route. J Biosci. 36, 153-161.doi: 10.1007/s12038-011-9009-1.
129. Vaucheret, H. (2006). Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20, 759-771.
130. Walker, W.B., and Allen, M.L. (2010). Expression and RNA interference of salivary polygalacturonase genes in the tarnished plant bug, Lygus lineolaris. J Insect Sci. 10, doi: 10.1673/031.010.14133.
131. Wang, S., Conant, G. C., Ou, R., and Beerntsen, B.T. (2012). Cloning and characterization of the peptidoglycan recognition protein genes in the mosquito, Armigeres subalbatus (Diptera: Culicidae). J Med Entomol. 49, 656-71.
132. Wang, Z., Dong, Y., Desneux, N., and Niu, C. (2013). RNAi Silencing of the HaHMG-CoA Reductase Gene Inhibits Oviposition in the Helicoverpa armigera Cotton Bollworm. PLoS One 8, e67732 doi:10.1371/journal.pone.0067732.
133. Wani, S. H., Sanghera, G.S., and Singh, G. S. (2010). Biotechnology and Plant Disease Control-Role of RNA Interference. Am J Plant Sci. 1, 55-68. doi:10.4236/ajps.2010.12008.
134. Warthmann, N., Chen, H., Ossowski, S., Weigel, D., and Herve, P. (2008). Highly specific gene silencing by artificial miRNAs in rice. PLoS One 3, 1-10. doi: 10.1371/journal.pone.0001829.
135. Waterhouse, P. M., and Helliwell, C.A. (2003). Exploring plant genomes by RNA-induced gene silencing. Nat Rev Genet. 4, 29-38. doi:10.1038/nrg982.
136. Wing, K. D., Schnee, M. E., Sacher, M., and Connair, M. (1998). A novel oxadiazine insecticide is bioactivated in lepidopteran larvae. Arch Insect Biochem Physiol. 3, 91-103. doi: 10.1002/ (SICI) 1520-6327.
137. Winston, W.M., Molodowitch, C., and Hunter, C.P. (2002). Systemic RNAi in C. elegans Requires the Putative Transmembrane Protein SID-1. Science 2456-2459. DOI:10.1126/science.1068836.
138. Xiong, Y., Zeng, H., Zhang, Y., Xu, D., and Qiu, D. (2013). Silencing the HaHR3 Gene by Transgenic Plant-mediated RNAi to Disrupt Helicoverpa armigera Development. Int J Biol Sci. 9, 370-381. doi:10.7150/ijbs.5929.
139. Xu, X., Jin, F., Yu, X., Ji, S., Wang, J., Cheng, H., et al. (2007). Expression and purification of a recombinant antibacterial peptide, cecropin, from Escherichia coli. Protein Expr Purif. 53, 293-301. doi: 10.1016/j.pep.2006.12.020.
140. Xu, P., Zhang, Y., Kang, L., Roossinck, M. J., and Mysore, K. S. (2006). Computational estimation and experimental verification of off-target silencing during posttranscriptional gene silencing in plants. Plant Physiol. 142, 429-440.
141. Xu, Y., Zou, Z., Zha, X., Xiang, Z., and He, N. (2012). A syntenic coding region for vitelline membrane proteins in four lepidopteran insects. J Mol Biochem. 1, 155-160.
142. Yan, J., Cheng, Q., Li C. B., and Aksoy, S. (2001). Molecular characterization of two serine proteases expressed in gut tissue of the African trypanosome vector, Glossina morsitans morsitans. Insect Mol Biol. 10, 47-56.
143. Yang, Z., Chen, J., Chen, Y., and Jiang, S. (2010). Molecular cloning and characterization of an acetylcholinesterase cDNA in the brown planthopper, Nilaparvata lugens. J Insect Sci. 10, 102. doi: 10.1673/031.010.10201.
144. Yao, J., Rotenberg, D., Afsharifar, A., Barandoc-Alviar, K., and Whitfield A. E. (2013). Development of RNAi Methods for Peregrinus maidis, the Corn Planthopper. PLoS One 8, e70243. doi:10.1371/journal.pone.0070243.
145. Yin, J., Feng, H., Sun, H., Xi, J., Cao, Y., and Li, K. (2012). Functional Analysis of General Odorant Binding Protein 2 from the Meadow Moth, Loxostege sticticalis L. (Lepidoptera: Pyralidae). PLoS One 7, e33589. doi:10.1371/journal.pone.0033589.
146. Yokoyama, H., Yokoyama, T., Yuasa, M., Fujimoto, H., Sakudoh, T., Honda, N., et al. (2013). Lipid transfer particle from the silkworm, Bombyx mori, is a novel member of the apoB/large lipid transfer protein family. J Lipid Res. 54, 2379-2390. doi: 10.1194/jlr.M037093.
147. You-Jin, H., Wen-Xia, H, U., and Bin, C. (2014). Comparative analysis of proteins in non-and summer-diapausing pupae of the onion fly, Delia antiqua (Diptera: Anthomyiidae), using twodimensional gel electrophoresis. Acta Entomol Sinica. 57, 161-167.
148. Yu, N., Christiaens, C., Liu, J., Niu, J., Cappelle, K., Caccia, S., et al. (2013). Delivery of dsRNA for RNAi in insects: an overview and future directions. Insect Sci. 20, 4-14 doi: 10.1111/j.1744- 7917.2012.01534.x.
149. Zalewska, M., Kochman, A., Estève, J. P., Lopez, F., Chaoui, K., Susini, C., et al. (2009). Juvenile hormone binding protein traffic - Interaction with ATP synthase and lipid transfer proteins. Biochim Biophys Acta.1788, 1695-1705.doi: 10.1016/j.bbamem.
150. Zamore, P. D., Tuschl, T., Shorp, P.A., and Bartel, D. P. (2000). RNAi: double stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101, 25-33.
151. Zha, W., Peng, X., Chen, R., Du, B., and Zhu, L. (2011). Knockdown of Midgut Genes by dsRNATransgenic Plant-Mediated RNA Interference in the Hemipteran Insect Nilaparvata lugens. PLoS One 6, e20504. doi:10.1371/journal.pone.0020504.
152. Zhang, J., Li, D., Ge, P., Guo, Y., and Zhu, K. Y. (2014). Molecular and Functional Characterization of cDNAs Putatively Encoding Carboxylesterases from the Migratory Locust, Locusta migratoria. PLoS One 9, e94809. doi:10.1371/journal.pone.0094809.
153. Zhang, X., Liu, X., Ma, J., and Zhao, J. (2013a). Silencing of cytochrome P450 CYP6B6 gene of cotton bollworm (Helicoverpa armigera) by RNAi. Bull Entomol Res. 103, 584-591. doi:10.1017/S0007485313000151.
154. Zhang, H., Li, H.C., Miao, X.X. (2013b). Feasibility, limitation and possible solutions of RNAi-based technology for insect pest control. Insect Sci. 20,15-30.
155. Zhao, H., Yi, X., Hu, Z., Hu, M., and Chen, S. (2013). RNAi-Mediated Knockdown of Catalase Causes Cell Cycle Arrest in SL-1 Cells and Results in Low Survival Rate of Spodoptera litura (Fabricius). PLoS One 8, e59527. doi: 10.1371/journal.pone.0059527.
156. Zhao, Y., Yang, G., Wang-Pruski, G., and You, M. (2008). Phyllotreta striolata (Coleoptera: Chrysomelidae): Arginine kinase cloning and RNAi-based pest control. Eur J. Entomol. 105, 815- 822.
157. Zhu, F., Sams, S., Moural, T., Haynes, K. F., Potter, M. F., and Palli, S. R. (2012). RNA interference of NADPH-cytochrome P450 reductase results in reduced insecticide resistance in the bed bug, Cimex lectularius. PLoS One 7, e31037. doi: 10.1371/journal.pone.0031037.
158. Zhu, Q., Arakane, Y., Beeman, R.W., Kramer, K.J., and Muthukrishnan, S. (2008). Functional specialization among insect chitinase family genes revealed by RNA interference. Proc Natl Acad Sci USA 105, 6650-5. doi: 10.1073/pnas.0800739105.