Small interfering RNA pathway modulates persistent infection of a plant virus in its insect vector

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Lan, Hanhong ^a   Wang, Haitao ^a   Chen, Qian ^a   Chen, Hongyan ^a   Jia, Dongsheng ^a   Mao, Qianzhuo ^a   Wei, Taiyun ^a  

^a FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE PROTEIN; INSECT PROTEIN; RNA HELICASE; SMALL INTERFERING RNA;

ANIMAL; COPY NUMBER VARIATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEMIPTERA; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INSECT VECTOR; ORYZA; PATHOGENICITY; PLANT DISEASE; REOVIRIDAE; VIROLOGY; VIRUS GENOME; VIRUS REPLICATION;

ANIMALS; ARGONAUTE PROTEINS; DNA COPY NUMBER VARIATIONS; GENOME, VIRAL; HEMIPTERA; HOST-PATHOGEN INTERACTIONS; INSECT PROTEINS; INSECT VECTORS; ORYZA; PLANT DISEASES; REOVIRIDAE; RNA HELICASES; RNA, SMALL INTERFERING; VIRUS REPLICATION;

EID: 84958568805     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep20699     Document Type: Article

References (47)

1. Goic, B. & Saleh, M. C. Living with the enemy: viral persistent infections from a friendly viewpoint. Curr. Opin. Microbiol. 15, 531-7 (2012).
2. Flegel, T. W. Update on viral accommodation, a model for host-viral interaction in shrimp and other arthropods. Dev. Comp. Immunol. 31, 217-31 (2007).
3. Roekring, S., Flegel, T. W., Malasit, P. & Kittayapong, P. Challenging successive mosquito generations with a densonucleosis virus yields progressive survival improvement but persistent, innocuous infections. Dev. Comp. Immunol. 30, 878-92 (2006).
4. Goic, B. et al. RNA-mediated interference and reverse transcription control the persistence of RNA viruses in the insect model Drosophila. Nat Immunol. 14, 396-403 (2013).
5. Blair, C. D. Mosquito RNAi is the major innate immune pathway controlling arbovirus infection and transmission. Future Microbiol. 6, 265-77 (2011).
6. Ding, S. W. RNA-based antiviral immunity. Nat. Rev. Immunol. 10, 632-44 (2010).
7. Donald, C. L., Kohl, A. & Schnettler, E. New insights into control of arbovirus replication and spread by insect RNA interference pathways. Insects 3, 511-31 (2012).
8. Fragkoudis, R., Attarzadeh-Yazdi, G., Nash, A. A., Fazakerley, J. K. & Kohl, A. Advances in dissecting mosquito innate immune responses to arbovirus infection. J Gen Virol. 90, 2061-72 (2009).
9. Myles, K. M., Wiley, M. R., Morazzani, E. M. & Adelman, Z. N. Alphavirus-derived small RNAs modulate pathogenesis in disease vector mosquitoes. Proc Natl Acad Sci USA 105, 19938-43 (2008).
10. Cirimotich, C. M., Scott, J. C., Phillips, A. T., Geiss, B. J. & Olson, K. E. Suppression of RNA interference increases alphavirus replication and virus-associated mortality in Aedes aegypti mosquitoes. BMC Microbiol. 9, 49 (2009).
11. Gammon, D. B. & Mello, C. C. RNA interference-mediated antiviral defense in insects. Curr Opin Insect Sci. 8, 111-20 (2015).
12. Bronkhorst, A. W. & van Rij, R. P. The long and short of antiviral defense: small RNA-based immunity in insects. Curr Opin Virol. 7, 19-28 (2014).
13. Hogenhout, S. A., Ammar, E. D., Whitfield, A. E. & Redinbaugh, M. G. Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol. 46, 327-59 (2008).
14. Wan, G. et al. Rice stripe virus counters reduced fecundity in its insect vector by modifying insect physiology, primary endosymbionts and feeding behavior. Sci Rep. 5, 12527 (2015).
15. Li, S. et al. Rice stripe virus affects the viability of its vector offspring by changing developmental gene expression in embryos. Sci Rep. 5, 7883 (2015).
16. Nakasuji, F. & Kiritani, K. Effects of Rice dwarf virus upon its vector, Nephotettix cincticeps uhler (Hemiptera: Deltocephalidae), and its significance for changes in relative abundance of infected individuals among vector populations. App. Ent. zool. 5, 1-12 (1970).
17. Tu, Z., Ling, B., Xu, D., Zhang, M. & Zhou, G. Effects of southern rice black-streaked dwarf virus on the development and fecundity of its vector, Sogatella furcifera. Virol J. 10, 145 (2013).
18. Lei, W., Liu, D., Li, P. & Hou, M. Interactive effects of southern rice black-streaked dwarf virus infection of host plant and vector on performance of the vector, Sogatella furcifera (Homoptera: Delphacidae). J Econ Entomol. 107, 1721-7 (2014).
19. Xu, Y., Zhou, W., Zhou, Y., Wu, j. & Zhou, X. Transcriptome and comparative gene expression analysis of Sogatella furcifera (Horváth) in response to southern rice black-streaked dwarf virus. PLoS One. 7, e36238 (2012).
20. Xu, Y., Huang, L. Z., Fu, S., Wu, J. X. & Zhou, X. P. Population diversity of rice stripe virus-derived siRNAs in three different hosts and RNAi-based antiviral immunity in Laodelphgax striatellus. PLoS One. 7, e46238 (2012).
21. Li, J. et al. Characterization of Rice black-streaked dwarf virus- and Rice stripe virus-derived siRNAs in singly and doubly infected insect vector Laodelphax striatellus. PLoS One. 8, e66007 (2013).
22. Omura, T. et al. Rice gall dwarf, a new virus disease. Plant Dis. 64, 795-7 (1980).
23. Putta, M., Chettanachit, D., Morinaka, T. & Parejarearn, D. Gall dwarf-new rice virus disease in Thailand. Int. Rice Res. Newslett. 5, 10-11 (1980).
24. Ong, C. A. & Omura, T. Rice gall dwarf virus occurrence in Peninsular Malaysia. Int. Rice Res. Newslett. 7, 7 (1982).
25. Fan, H. et al. Rice gall dwarf: a new virus disease epidemic in the west of Guangdong province of south China. Acta Phytopathol. Sin. 13, 1-6 (1983).
26. Zheng, L., Chen, H., Liu, H., Xie, L. & Wei, T. Assembly of viroplasms by viral nonstructural protein Pns9 is essential for persistent infection of rice gall dwarf virus in its insect vector. Virus Res. 196, 162-9 (2015).
27. Fan, G. C. et al. Expression of rice gall dwarf virus outer coat protein gene (S8) in insect cells. Virol. Sin. 25, 401-8 (2010).
28. Zhang, H. et al. Completion of the genome sequence of rice gall dwarf virus from Guangxi, China. Arch. Virol. 153, 1737-41 (2008).
29. Akita, F. et al. Viroplasm matrix protein Pns9 from rice gall dwarf virus forms an octameric cylindrical structure. J Gen Virol. 92, 2214-21 (2011).
30. Chen, H. et al. Rice gall dwarf virus exploits tubules to facilitate viral spread among cultured insect cells derived from leafhopper Recilia dorsalis. Front Microbiol. 4, 206 (2013).
31. Aliyari, R. et al. Mechanism of induction and suppression of antiviral immunity directed by virus-derived small RNAs in Drosophila. Cell Host Microbe. 4, 387-97 (2008).
32. Miesen, P., Girardi, E. & van Rij, R. P. Distinct sets of PIWI proteins produce arbovirus and transposon-derived piRNAs in Aedes aegypti mosquito cells. Nucleic Acids Res. 43, 6545-56 (2015).
33. Morazzani, E. M., Wiley, M. R., Murreddu, M. G., Adelman, Z. N. & Myles, K. M. Production of virus-derived ping-pong-dependent piRNA-like small RNAs in the mosquito soma. PLoS Pathog. 8, e1002470 (2012).
34. Chen, Y., Redinbaugh, M. G. & Michel, A. P. Molecular interactions and immune responses between Maize fine streak virus and the leafhopper vector Graminella nigrifrons through differential expression and RNA interference. Insect Mol Biol. 24, 391-401 (2015).
35. Whitfield, A. E., Falk, B. W. & Rotenberg, D. Insect vector-mediated transmission of plant viruses. Virology. 479-480, 278-89 (2015).
36. Hohn, T. Plant virus transmission from the insect point of view. Proc Natl Acad Sci USA 104, 17905-06 (2007).
37. Oliveira, V. C. et al. A silencing suppressor protein (NSs) of a tospovirus enhances baculovirus replication in permissive and semipermissive insect cell lines. Virus Res. 155, 259-67 (2011).
38. Hemmes, H., Lakatos, L., Goldbach, R., Burgyán, J. & Prins, M. The NS3 protein of Rice hoja blanca tenuivirus suppresses RNA silencing in plant and insect hosts by efficiently binding both siRNAs and miRNAs. RNA. 13, 1079-89 (2007).
39. Wu, J. et al. Identification of Pns12 as the second silencing suppressor of Rice gall dwarf virus. Sci China Life Sci. 54, 201-8 (2011).
40. Shen, W. J., Ruan, X. L., Li, X. S., Zhao, Q. & Li, H. P. RNA silencing suppressor Pns11 of rice gall dwarf virus induces virus-like symptoms in transgenic rice. Arch Virol. 157, 1531-9 (2012).
41. Wei, T. et al. Association of Rice gall dwarf virus with microtubules is necessary for viral release from cultured insect vector cells. J Virol. 83, 10830-5 (2009).
42. Jia, D. et al. Development of an insect vector cell culture and RNA interference system to investigate the functional role of fijivirus replication protein. J Virol. 86, 5800-7 (2012).
43. Mao, Q. et al. New model for the genesis and maturation of viroplasms induced by fijiviruses in insect vector cells. J Virol. 87, 6819-28 (2013).
44. Jia, D. et al. Virus-induced tubule: a vehicle for rapid spread of virions through basal lamina from midgut epithelium in the insect vector. J Virol. 88, 10488-500 (2014).
45. Xu, H. J. et al. Genome-wide screening for components of small interfering RNA (siRNA) and micro-RNA (miRNA) pathways in the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Insect Mol. Biol. 22, 635-47 (2013).
46. Huo, Y. et al. Transovarial transmission of a plant virus is mediated by vitellogenin of its insect vector. PLoS Pathog. 10, e1003949 (2014).
47. Liu, S., Ding, Z., Zhang, C., Yang, B. & Liu, Z. Gene knockdown by intro-thoracic injection of double-stranded RNA in the brown planthopper, Nilaparvata lugens. Insect Biochem Mol Biol. 40, 666-71 (2010).