Instar-dependent systemic RNA interference response in Leptinotarsa decemlineata larvae

Pesticide Biochemistry and Physiology

Volumn 123, Issue , 2015, Pages 64-73

  Guo, Wen Chao ^a,b   Fu, Kai Yun ^a   Yang, Shuai ^b   Li, Xiao Xu ^b   Li, Guo Qing ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF MICROBIOLOGY   (China)

Author keywords

Argonaute; Dicer; Leptinotarsa decemlineata; RNA interference efficiency

Indexed keywords

LEPTINOTARSA DECEMLINEATA;

ADENOSYLHOMOCYSTEINASE; ARGONAUTE PROTEIN; INSECT PROTEIN; RIBONUCLEASE III;

ANIMAL; BEETLE; BIOSYNTHESIS; GENETICS; LARVA; METABOLISM; RNA INTERFERENCE;

ADENOSYLHOMOCYSTEINASE; ANIMALS; ARGONAUTE PROTEINS; BEETLES; INSECT PROTEINS; LARVA; RIBONUCLEASE III; RNA INTERFERENCE;

EID: 84938988474     PISSN: 00483575     EISSN: 10959939     Source Type: Journal    
DOI: 10.1016/j.pestbp.2015.03.006     Document Type: Article

References (65)

1. Meister G., Tuschl T. Mechanisms of gene silencing by double-stranded RNA. Nature 2004, 431:343-349.
2. Elbashir S.M., Lendeckel W., Tuschl T. RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev 2001, 15:188-200.
3. Elbashir S.M., Harborth J., Lendeckel W., Yalcin A., Weber K., Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001, 411:494-498.
4. Zamore P.D., Tuschl T., Sharp P.A., Bartel D.P. RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 2000, 101:25-33.
5. Hammond S.M., Bernstein E., Beach D., Hannon G.J. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 2000, 404:293-296.
6. Nykänen A., Haley B., Zamore P.D. ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 2001, 107:309-321.
7. Tomari Y., Zamore P.D. Perspective: machines for RNAi. Genes Dev 2005, 19:517-529.
8. Tomoyasu Y., Miller S.C., Tomita S., Schoppmeier M., Grossmann D., Bucher G. Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biol 2008, 9:R10.
9. Wynant N., Verlinden H., Breugelmans B., Simonet G., Vanden Broeck J. Tissue-dependence and sensitivity of the systemic RNA interference response in the desert locust, Schistocerca gregaria. Insect Biochem. Mol. Biol 2012, 42:911-917.
10. 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.
11. Belles X. Beyond Drosophila: RNAi in vitro and functional genomics in insects. Annu. Rev. Entomol 2010, 55:111-128.
12. Wynant N., Santos D., Vanden Broeck J. Biological mechanisms determining the success of RNA interference in insects. Int. Rev. Cell Mol. Biol 2014, 312:139-167.
13. 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.
14. 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.
15. Price D.R., Gatehouse J.A. RNAi-mediated crop protection against insects. Trends Biotechnol 2008, 26:393-400.
16. Amdam G.V., Simões Z.L., Guidugli K.R., Norberg K., Omholt S.W. Disruption of vitellogenin gene function in adult honeybees by intra-abdominal injection of double-stranded RNA. BMC Biotechnol 2003, 3:1.
17. Yang J., Han Z.-J. Efficiency of different methods for dsRNA delivery in cotton bollworm (Helicoverpa armigera). J. Integr. Agric 2014, 13:115-123.
18. Ren X.-L., Ma Y., Cui J.-J., Li G.-Q. RNA interference-mediated knockdown of three putative aminopeptidases N affects susceptibility of Spodoptera exigua larvae to Bacillus thuringiensis Cry1Ca. J. Insect Physiol 2014, 67:28-36.
19. Zhou L.-T., Jia S., Wan P.-J., Kong Y., Guo W.-C., Ahmat T., et al. RNA interference of a putative S-adenosyl-L-homocysteine hydrolase gene affects larval performance in Leptinotarsa decemlineata (Say). J. Insect Physiol 2013, 59:1049-1056.
20. 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 to Cry1Ca and Cry1Ac toxicity. Appl. Environ. Microbiol 2013, 79:5576-5583.
21. Zhu F., Xu J., Palli R., Ferguson J., Palli S.R. Ingested RNA interference for managing the populations of the Colorado potato beetle, Leptinotarsa decemlineata. Pest Manag. Sci 2011, 67:175-182.
22. Tian H., Peng H., Yao Q., Chen H., Xie Q., Tang B., et al. Developmental control of a lepidopteran pest Spodoptera exigua by ingestion of bacteria expressing dsRNA of a non-midgut gene. PLoS ONE 2009, 4. e6225.
23. Luo Y., 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.
24. Liu J., Smagghe G., Swevers L. Transcriptional response of BmToll9-1 and RNAi machinery genes to exogenous dsRNA in the midgut of Bombyx mori. J. Insect Physiol 2013, 59:646-654.
25. Wan P.J., Lü D., Guo W.C., Ahmat T., Yang L., Mu L.L., et al. Molecular cloning and characterization of a putative proline dehydrogenase gene in the Colorado potato beetle, Leptinotarsa decemlineata (Say). Insect Sci 2014, 21:147-158.
26. 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.
27. Zheng W., Zhu C., Peng T., Zhang H. Odorant receptor co-receptor Orco is upregulated by methyl eugenol in male Bactrocera dorsalis (Diptera: Tephritidae). J. Insect Physiol 2012, 58:1122-1127.
28. Wan P.-J., Guo W.-Y., Yang Y., Lü 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.
29. Wan P.-J., Fu K.-Y., Lü F.-G., Guo W.-C., Li G.-Q. A putative δ1-pyrroline-5-carboxylate synthetase involved in the biosynthesis of proline and arginine in Leptinotarsa decemlineata. J. Insect Physiol 2014, 71:105-113.
30. Fu K.-Y., Guo W.-C., Lü F.-G., Liu X.-P., Li G.-Q. Response of the vacuolar ATPase subunit E to RNA interference and four chemical pesticides in Leptinotarsa decemlineata. Pestic. Biochem. Physiol 2014, 114:16-23.
31. Kong Y., Liu X.-P., Wan P.-J., Shi X.-Q., Guo W.-C., Li G.-Q. The P450 enzyme Shade mediates the hydroxylation of ecdysone to 20-hydroxyecdysone in the Colorado potato beetle, Leptinotarsa decemlineata. Insect Mol. Biol 2014, 23:632-643.
32. Liu X.-P., Fu K.-Y., Lü F.-G., Meng Q.-W., Guo W.-C., Li G.-Q. Involvement of FTZ-F1 in the regulation of pupation in Leptinotarsa decemlineata (Say). Insect Biochem. Mol. Biol 2014, 55:51-60.
33. Meng Q.-W., Liu X.-P., Lü F.-G., Fu K.-Y., Guo W.-C., Li G.-Q. Involvement of a putative allatostatin in regulation of juvenile hormone titer and the larval development in Leptinotarsa decemlineata (Say). Gene 2015, 554:105-113.
34. Swevers L., Huvenne H., Menschaert G., Kontogiannatos D., Kourti A., Pauchet Y., et al. Colorado potato beetle (Coleoptera) gut transcriptome analysis: expression of RNA interference-related genes. Insect Mol. Biol 2013, 22:668-684.
35. Shi X.-Q., Guo W.-C., Wan P.-J., Zhou L.-T., Ren X.-L., Tursun A., et al. Validation of reference genes for expression analysis by quantitative real-time PCR in Leptinotarsa decemlineata (Say). BMC Res. Notes 2013, 6:93.
36. Kumar A., Congiu L., Lindström L., Piiroinen S., Vidotto M., Grapputo A. Sequencing, de novo assembly and annotation of the Colorado potato beetle, Leptinotarsa decemlineata, transcriptome. PLoS ONE 2014, 9. e86012.
37. Kontogiannatos D., Swevers L., Maenaka K., Park E.Y., Iatrou K., Kourti A. Functional characterization of a juvenile hormone esterase related gene in the moth Sesamia nonagrioides through RNA interference. PLoS ONE 2013, 8. e73834.
38. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
39. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol 2013, 30:2725-2729.
40. Abbott W. A method of computing the effectiveness of an insecticide. J. Econ. Entomol 1925, 18:265-267.
41. Carmell M.A., Hannon G.J. RNase III enzymes and the initiation of gene silencing. Nat. Struct. Mol. Biol 2004, 11:214-218.
42. Bernstein E., Caudy A.A., Hammond S.M., Hannon G.J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001, 409:363-366.
43. Lee Y.S., Nakahara K., Pham J.W., Kim K., He Z., Sontheimer E.J., et al. Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 2004, 117:69-81.
44. Jaubert-Possamai S., Rispe C., Tanguy S., Gordon K., Walsh T., Edwards O., et al. Expansion of the miRNA pathway in the hemipteran insect Acyrthosiphon pisum. Mol. Biol. Evol 2010, 27:979-987.
45. Okamura K., Ishizuka A., Siomi H., Siomi M.C. Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways. Genes Dev 2004, 18:1655-1666.
46. Yigit E., Batista P.J., Bei Y., Pang K.M., Chen C.C., Tolia N.H., et al. Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell 2006, 127:747-757.
47. Bansal R., Michel A.P. Core RNAi machinery and Sid1, a component for systemic RNAi, in the hemipteran insect, Aphis glycines. Int. J. Mol. Sci 2013, 14:3786-3801.
48. Parker J.S., Barford D. Argonaute: a scaffold for the function of short regulatory RNAs. Trends Biochem. Sci 2006, 31:622-630.
49. Ma J., Ye K., Patel D.J. Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 2004, 429:318-322.
50. Elkayam E., Kuhn C.D., Tocilj A., Haase A.D., Greene E.M., Hannon G.J., et al. The structure of human Argonaute-2 in complex with miR-20a. Cell 2012, 150:100-110.
51. Singh A.D., Wong S., Ryan C.P., Whyard S. Oral delivery of double-stranded RNA in larvae of the yellow fever mosquito, Aedes aegypti: implications for pest mosquito control. J. Insect Sci 2013, 13:69.
52. Wan P.-J., Jia S., Li N., Fan J.-M., Li G.-Q. RNA interference depletion of the Halloween gene Disembodied implies its potential application for management of planthopper Sogatella furcifera and Laodelphax striatellus. PLoS ONE 2014, 9. e86675.
53. Garbutt J.S., Reynolds S.E. Induction of RNA interference genes by double-stranded RNA; implications for susceptibility to RNA interference. Insect Biochem. Mol. Biol 2012, 42:621-628.
54. Chen Y.-H., Jia X.-T., Zhao L., Li C.-Z., Zhang S., Chen Y.-G., et al. Identification and functional characterization of Dicer2 and five single VWC domain proteins of Litopenaeus vannamei. Dev. Comp. Immunol 2011, 35:661-671.
55. Su J., Zhu Z., Wang Y., Zou J., Wang N., Jang S. Grass carp reovirus activates RNAi pathway in rare minnow, Gobiocypris rarus. Aquaculture 2009, 289:1-5.
56. Christiaens O., Swevers L., Smagghe G. DsRNA degradation in the pea aphid (Acyrthosiphon pisum) associated with lack of response in RNAi feeding and injection assay. Peptides 2014, 53:307-314.
57. Swevers L., Liu J., Huvenne H., Smagghe G. Search for limiting factors in the RNAi pathway in silkmoth tissues and the Bm5 cell line: the RNA-binding proteins R2D2 and Translin. PLoS ONE 2011, 6. e20250.
58. Calixto A., Chelur D., Topalidou I., Chen X.Y., Chalfie M. Enhanced neuronal RNAi in C. elegans using SID-1. Nat. Methods 2010, 7:554-559.
59. Diederichs S., Jung S., Rothenberg S.M., Smolen G.A., Mlody B.G., Haber D.A. Coexpression of Argonaute-2 enhances RNA interference toward perfect match binding sites. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:9284-9289.
60. Arimatsu Y., Kotani E., Sugimura Y., Furusawa T. Molecular characterization of a cDNA encoding extracellular dsRNase and its expression in the silkworm, Bombyx mori. Insect Biochem. Mol. Biol 2007, 37:176-183.
61. Wynant N., Santos D., Verdonck R., Spit J., Van Wielendaele P., Broeck J.V. 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.
62. Liu J., Swevers L., Iatrou K., Huvenne H., Smagghe G. Bombyx mori DNA/RNA non-specific nuclease: expression of isoforms in insect culture cells, subcellular localization and functional assays. J. Insect Physiol 2012, 58:1166-1176.
63. Allen M.L., Walker W.B. Saliva of Lygus lineolaris digests double stranded ribonucleic acids. J. Insect Physiol 2012, 58:391-396.
64. Garbutt J.S., Bellés X., Richards E.H., Reynolds S.E. Persistence of double-stranded RNA in insect hemolymph as a potential determiner of RNA interference success: evidence from Manduca sexta and Blattella germanica. J. Insect Physiol 2013, 59:171-178.
65. Kennedy S., Wang D., Ruvkun G. A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 2004, 427:645-649.