Ingestion of genetically modified yeast symbiont reduces fitness of an insect pest via RNA interference

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Murphy, Katherine A ^a   Tabuloc, Christine A ^a   Cervantes, Kevin R ^a   Chiu, Joanna C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; GENE; GENETICS; GROWTH, DEVELOPMENT AND AGING; INSECT; LARVA; PHYSIOLOGY; RNA INTERFERENCE; SACCHAROMYCES CEREVISIAE; SYMBIOSIS;

ANIMALS; GENES, INSECT; INSECTS; LARVA; RNA INTERFERENCE; SACCHAROMYCES CEREVISIAE; SYMBIOSIS;

EID: 84960193436     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep22587     Document Type: Article

References (66)

1. Coy, M. R. et al. Gene silencing in adult Aedes aegypti mosquitoes through oral delivery of double-stranded RNA. J. Appl. Entomol. 136, 741-748 (2012).
2. Jarosch, A., Moritz, R. F. Systemic RNA-interference in the honeybee Apis mellifera: Tissue dependent uptake of fluorescent siRNA after intra-abdominal application observed by laser-scanning microscopy. J. Insect Physiol. 57, 851-857 (2011).
3. Li, H. et al. Long dsRNA but not siRNA initiates RNAi in western corn rootworm larvae and adults. J. Appl. Entomol. 139, 432-445 (2015).
4. Zhang, J., Khan, S. A., Hasse, C., Ruf, S. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science. 347, 991-994 (2015).
5. Copeland, J. M. et al. Extension of Drosophila life span by RNAi of the mitochondrial respiratory chain. Curr. Biol. 19, 1591-1598 (2009).
6. Baum, J. a. et al. Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 25, 1322-1326 (2007).
7. 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. 6, 1-7 (2006).
8. Zhou, X., Wheeler, M. M., Oi, F. M., Scharf, M. E. RNA interference in the termite Reticulitermes flavipes through ingestion of double-stranded RNA. Insect Biochem. Mol. Biol. 38, 805-815 (2008).
9. Zhang, H., Li, H., Guan, R., Miao, X. Lepidopteran insect species-specific, broad-spectrum, and systemic RNA interference by spraying dsRNA on larvae. Entomol. Exp. Appl. 155, 218-228 (2015).
10. Chen, A., Zheng, W., Zheng, W., Zhang, H. The effects of RNA interference targeting Bactrocera dorsalis ds-Bdrpl19 on the gene expression of rpl19 in non-target insects. Ecotoxicology 24, 595-603 (2015).
11. Obbard, D. J., Gordon, K. H. J., Buck, A. H., Jiggins, F. M. The evolution of RNAi as a defence against viruses and transposable elements. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 364, 99-115 (2009).
12. Kim, D. H., Rossi, J. J. RNAi mechansims and applications. Biotechniques. 44, 613-616 (2009).
13. Belles, X. Beyond Drosophila: RNAi in vivo and functional genomics in insects. Annu. Rev. Entomol. 55, 111-128 (2010).
14. Zotti, M. J., Smagghe, G. RNAi technology for insect management and protection of beneficial insects from diseases: lessons, challenges and risk assessments. Neotrop. Entomol. 44, 107-213 (2015).
15. Burand, J. P., Hunter, W. B. RNAi: Future in insect management. J. Invertebr. Pathol. 112, S68-74 (2013).
16. Gordon, K. H. J., Waterhouse, P. M. RNAi for insect-proof plants. Nat. Biotechnol. 25, 1231-1232 (2007).
17. Saleh, M. et al. The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Cell 8, 793-802 (2009).
18. Dzitoyeva, S., Dimitrijevic, N., Manev, H. Intra-abdominal injection of double-stranded RNA into anesthetized adult Drosophila triggers RNA interference in the central nervous system. Mol Psychiatry 6, 665-670 (2001).
19. Caplen, N. J., Fleenor, J., Fire, A., Morgan, R. A. dsRNA-mediated gene silencing in cultured Drosophila cells: a tissue culture model for the analysis of RNA interference. Gene 252, 95-105 (2000).
20. Whyard, S., Singh, A. D., Wong, S. Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochem. Mol. Biol. 39, 824-832 (2009).
21. Mao, Y. B. et al. Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat. Biotechnol. 25, 1307-1313 (2007).
22. San Miguel, K., Scott, J. G. The next generation of insecticides: dsRNA is stable as a foliar-applied insecticide. Pest Manag. Sci. Epub ahead of print. (2015). doi: 10.1002/ps.4056.
23. Li, H., Guan, R., Guo, H., Miao, X. New insights into an RNAi approach for plant defence against piercing-sucking and stem-borer insect pests. Plant. Cell Environ. Epub ahead of print. (2015). doi: 10.1111/pce.12546.
24. 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. 19, 683-693 (2010).
25. Tian, H. et al. Developmental control of a lepidopteran pest Spodoptera exigua by ingestion of bacteria expressing dsRNA of a nonmidgut gene. PLoS One 4, e6225 (2009).
26. 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. 67, 175-182 (2011).
27. Taracena, M. L. et al. Genetically modifying the insect gut microbiota to control Chagas disease vectors through systemic RNAi. PLoS Negl. Trop. Dis. 9, e0003358 (2015).
28. Starmer, W. T. A Comparison of Drosophila habitats according to the physiological attributes of the associated yeast communities. Soc. Study Evol. 35, 38-52 (1981).
29. Becher, P. G. et al. Yeast, not fruit volatiles mediate Drosophila melanogaster attraction, oviposition and development. Funct. Ecol. 26, 822-828 (2012).
30. Scheidler, N. H., Liu, C., Hamby, K. A., Zalom, F. G., Syed, Z. Volatile codes: Evolution of olfactory signals and reception in Drosophila-yeast chemical communication. Sci. Rep. 5, 14059 (2015).
31. Palanca, L., Gaskett, A. C., Gunther, C. S., Newcomb, R. D., Goddard, M. R. Quantifying variation in the ability of yeasts to attract Drosophila melanogaster. PLoS One 8, e75332 (2013).
32. Harrison, B. R., Yazgan, O., Krebs, J. E. Life without RNAi: noncoding RNAs and their functions in Saccharomyces cerevisiae. Biochem. Cell Biol. 87, 767-779 (2009).
33. Starmer, W. T., Peris, F., Fontdevila, A. The transmission of yeasts by Drosophila buzzatii during courtship and mating. Anim. Behav. 36, 1691-1695 (1988).
34. Coluccio, A. E., Rodriguez, R. K., Kernan, M. J., Neiman, A. M. The yeast spore wall enables spores to survive passage through the digestive tract of Drosophila. PLoS One 3, e2873 (2008).
35. Lee, J. C. et al. The susceptibility of small fruits and cherries to the spotted-wing Drosophila, Drosophila suzukii. Pest Manag. Sci. 67, 1358-1367 (2011).
36. Asplen, M. K., Anfora, G., Biondi, A. Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest SC 88, 469-494 (2015).
37. Walsh, D. B. et al. Drosophila suzukii (Diptera: Drosophilidae): Invasive pest of ripening soft fruit expanding its geographic range and damage potential. J. Integr. Pest Manag. 2, 1-7 (2011).
38. Bolda, M. P., Goodhue, R. E., Zalom, F. G. Spotted Wing Drosophila: Potential economic impact of a newly established pest. Agric. Resour. Econ. Updat. Univ. California. Giannini Found. 13, 5-8 (2010).
39. Chiu, J. C. et al. Genome of Drosophila suzukii, the Spotted Wing Drosophila. G3-Genes Genomes Genet. 3, 2257-2271 (2013).
40. Iglesias, L. E., Nyoike, T. W., Liburd, O. E. Effect of trap design, bait type, and age on captures of Drosophila suzukii (Diptera: Drosophilidae) in berry crops. Hortic. Entomol. 107, 1508-1518 (2014).
41. Hamby, K. A., Hernandez, A., Boundy-Mills, K., Zalom, F. G. Associations of yeasts with spotted-wing Drosophila (Drosophila suzukii; Diptera: Drosophilidae) in cherries and raspberries. Appl. Environ. Microbiol. 78, 4869-4873 (2012).
42. Mao, J., Zeng, F. Feeding-based RNA intereference of a gap gene is lethal to the pea aphid, Acyrthosiphon pisum. PLoS One 7, e48718 (2012).
43. Walshe, D. P., Lehane, S. M., Lehane, M. J., Haines, L. R. Prolonged gene knockdown in the tsetse fly Glossina by feeding double stranded RNA. Insect Mol. Biol. 18, 11-19 (2009).
44. Wuriyanghan, H., Rosa, C., Falk, B. W. Oral delivery of double-stranded RNAs and siRNAs induces RNAi effects in the potato/tomato psyllid, Bactericerca cockerelli. PLoS One 6, e27736 (2011).
45. Jackson, A. L., Linsley, P. S. Noise amidst the silence: Off-target effects of siRNAs Trends Genet. 20, 521-524 (2004).
46. Lundgren, J. G., Duan, J. J. RNAi-based insecticidal crops: potential effects on nontarget species. Bioscience 63, 657-665 (2013).
47. Altschul, S., Gish, W., Miller, W. Basic local alignment search tool. J Mol Biol. 215, 403-410 (1990).
48. Roignant, J.-Y. et al. Absence of transitive and systemic pathways allows cell-specific and isoform-specific RNAi in Drosophila. RNA 9, 299-308 (2003).
49. Haynes, K. F. Sublethal effects of neurotoxic insectidices on insect behavior. Annu. Rev. Entomol. 33, 149-168 (1988).
50. Robbins, M., Judge, A., MacLachlan, I. siRNA and innate immunity. Oligonucleotides 19, 89-102 (2009).
51. Wang, J., Lu, Z., Wientjes, M. G., Au, J. L.-S. Delivery of siRNA therapeutics: barriers and carriers. AAPS J. 12, 492-503 (2010).
52. McIsaac, R. S., Gibney, P. A., Chandran, S. S., Benjamin, K. R., Botstein, D. Synthetic biology tools for programming gene expression without nutritional perturbations in Saccharomyces cerevisiae. Nucleic Acids Res. 42, e48 (2014).
53. Lopez, G., Anderson, J. C. Synthetic auxotrophs with ligand-dependent essential genes for a BL21(DE3) biosafety strain. ACS Synth. Biol. 4, 1279-1286 (2015).
54. Rovner, A. J. et al. Recoded organisms engineered to depend on synthetic amino acids. Nature. 518, 89-93 (2015).
55. Hokanson, K. E., Dawson, W. O., Handler, A. M., Schetelig, M. F., S. Leger, R. J. Not all GMOs are crop plants: non-plant GMO applications in agriculture. Transgenic Res. 23, 1057-1068 (2013). doi: 10.1007/s11248-013-9769-5.
56. Ulrich, J. et al. Large scale RNAi screen in Tribolium reveals novel target genes for pest control and the proteasome as prime target. BMC Genomics 16, 674 (2015).
57. Gonzalez, F. Symbiosis between yeasts and insects. Introd. Pap. Fac. Landsc. Archit. Horiculture, Crop Prod. Sci. 1-52 (2014).
58. Svoboda, P. Off-targeting and other non-specific effects of RNAi experiments in mammalian cells. Curr. Opin. Mol. Ther. 9, 248-257 (2007).
59. Lemaire, P. A., Anderson, E., Lary, J., Cole, J. L. Mechanism of PKR activation by dsRNA. J Mol Biol. 381, 351-360 (2008).
60. Valcu, M., Valcu, C. M. Data transformation practices in biomedical sciences. Nat. Methods 8, 104-105 (2011).
61. Chintapalli, V. R., Wang, J., Dow, J. A. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat. Genet. 39, 715-720 (2007).
62. Larkin, M. a. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (2007).
63. Boutros, M. et al. Genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 303, 832-835 (2004).
64. Chiu, J. C., Low, K. H., Pike, D. H., Yildirim, E., Edery, I. Assaying locomotor activity to study circadian rhythms and sleep parameters in Drosophila. J. Vis. Exp. 28, 1-8 (2010). doi: 10.3791/2157.
65. Livak, K. J., Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2 CT method. Methods 25, 402-408 (2001).
66. Majercak, J., Chen, W., Edery, I. Splicing of the period gene 3 terminal intron is regulated by light, circadian clock factors, and phospholipase C. 24, 3359-3372 (2004).