The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Suppression of Rice Stripe Virus Replication in Laodelphax striatellus Using Vector Insect-Derived Double-Stranded RNAs

  • Fang, Ying (Department of Agricultural Biotechnology, College of Agriculture & Life Science, Seoul National University) ;
  • Choi, Jae Young (Department of Agricultural Biotechnology, College of Agriculture & Life Science, Seoul National University) ;
  • Park, Dong Hwan (Department of Agricultural Biotechnology, College of Agriculture & Life Science, Seoul National University) ;
  • Park, Min Gu (Department of Agricultural Biotechnology, College of Agriculture & Life Science, Seoul National University) ;
  • Kim, Jun Young (Department of Agricultural Biotechnology, College of Agriculture & Life Science, Seoul National University) ;
  • Wang, Minghui (Department of Agricultural Biotechnology, College of Agriculture & Life Science, Seoul National University) ;
  • Kim, Hyun Ji (Department of Agricultural Biotechnology, College of Agriculture & Life Science, Seoul National University) ;
  • Kim, Woo Jin (Department of Agricultural Biotechnology, College of Agriculture & Life Science, Seoul National University) ;
  • Je, Yeon Ho (Department of Agricultural Biotechnology, College of Agriculture & Life Science, Seoul National University)
  • Received : 2020.03.13
  • Accepted : 2020.05.06
  • Published : 2020.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

RNA interference (RNAi) has attracted attention as a promising approach to control plant viruses in their insect vectors. In the present study, to suppress replication of the rice stripe virus (RSV) in its vector, Laodelphax striatellus, using RNAi, dsRNAs against L. striatellus genes that are strongly upregulated upon RSV infection were delivered through a rice leaf-mediated method. RNAi-based silencing of peroxiredoxin, cathepsin B, and cytochrome P450 resulted in significant down regulation of the NS3 gene of RSV, achieving a transcriptional reduction greater than 73.6% at a concentration of 100 ng/μl and, possibly compromising viral replication. L. striatellus genes might play crucial roles in the transmission of RSV; transcriptional silencing of these genes could suppress viral replication in L. striatellus. These results suggest effective RNAi-based approaches for controlling RSV and provide insight into RSV-L. striatellus interactions.

Keywords

References

  1. An, S. B., Choi, J. Y., Lee, S. H., Fang, Y., Kim, J. H., Park, D. H., Park, M. G., Woo, R. M., Kim, W. J. and Je, Y. H. 2017. Silencing of rice stripe virus in Laodelphax striatellus using virus-derived double-stranded RNAs. J. Asia-Pac. Entomol. 20:695-698. https://doi.org/10.1016/j.aspen.2017.04.009
  2. Bass, C., Carvalho, R. A., Oliphant, L., Puinean, A. M., Field, L. M., Nauen, R., Williamson, M. S., Moores, G. and Gorman, K. 2011. Overexpression of a cytochrome P450 monooxygenase, CYP6ER1, is associated with resistance to imidacloprid in the brown planthopper, Nilaparvata lugens. Insect Mol. Biol. 20:763-773. https://doi.org/10.1111/j.1365-2583.2011.01105.x
  3. Bolger, A. M., Lohse, M. and Usadel, B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114-2120. https://doi.org/10.1093/bioinformatics/btu170
  4. David, J.-P., Ismail, H. M., Chandor-Proust, A. and Paine, M. J. I. 2013. Role of cytochrome P450s in insecticide resistance: impact on the control of mosquito-borne diseases and use of insecticides on Earth. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368:20120429. https://doi.org/10.1098/rstb.2012.0429
  5. de Haro, L. A., Dumon, A. D., Mattio, M. F., Arguello Caro, E. B., Llauger, G., Zavallo, D., Blanc, H., Mongelli, V. C., Truol, G., Saleh, M.-C., Asurmendi, S. and del Vas, M. 2017. Mal de Rio Cuarto virus infection triggers the production of distinctive viral-derived siRNA profiles in wheat and its planthopper vector. Front. Plant Sci. 8:766. https://doi.org/10.3389/fpls.2017.00766
  6. Elzaki, M. E. A., Zhang, W., Feng, A., Qiou, X., Zhao, W. and Han, Z. 2016. Constitutive overexpression of cytochrome P450 associated with imidacloprid resistance in Laodelphax striatellus (Fallen). Pest Manag. Sci. 72:1051-1058. https://doi.org/10.1002/ps.4155
  7. Fang, Y., Choi, J. Y., Lee, S. H., Kim, J. H., Park, D. H., Park, M. G., Woo, R. M., Lee, B. R., Kim, W. J., Li, S. and Je, Y. H. 2017. RNA interference of E75 nuclear receptor gene suppresses transmission of rice stripe virus in Laodelphax striatellus. J. Asia-Pac. Entomol. 20:1140-1144. https://doi.org/10.1016/j.aspen.2017.08.011
  8. Feyereisen, R. 2015. Insect P450 inhibitors and insecticides: challenges and opportunities. Pest Manag. Sci. 71:793-800. https://doi.org/10.1002/ps.3895
  9. Galiana-Arnoux, D., Dostert, C., Schneemann, A., Hoffmann, J. A. and Imler, J.-L. 2006. Essential function in vivo for Dicer-2 in host defense against RNA viruses in drosophila. Nat. Immunol. 7:590-597. https://doi.org/10.1038/ni1335
  10. Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., di Palma, F., Birren, B. W., Nusbaum, C., Lindblad-Toh, K., Friedman, N. and Regev, A. 2011. Fulllength transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29:644-652. https://doi.org/10.1038/nbt.1883
  11. Hamamatsu, C., Toriyama, S., Toyoda, T. and Ishihama, A. 1993. Ambisense coding strategy of the rice stripe virus genome: in vitro translation studies. J. Gen. Virol. 74:1125-1131. https://doi.org/10.1099/0022-1317-74-6-1125
  12. Hibino, H. 1996. Biology and epidemiology of rice viruses. Annu. Rev. Phytopathol. 34:249-274. https://doi.org/10.1146/annurev.phyto.34.1.249
  13. Hogenhout, S. A., Ammar, E.-D., Whitfield, A. E. and Redinbaugh, M. G. 2008. Insect vector interactions with persistently transmitted viruses. Annu. Rev. Phytopathol. 46:327-359. https://doi.org/10.1146/annurev.phyto.022508.092135
  14. Ishikawa, K., Omura, T. and Hibino, H. 1989. Morphological characteristics of rice stripe virus. J. Gen. Virol. 70:3465-3468. https://doi.org/10.1099/0022-1317-70-12-3465
  15. Jaattela, M. and Tschopp, J. 2003. Caspase-independent cell death in T lymphocytes. Nat. Immunol. 4:416-423. https://doi.org/10.1038/ni0503-416
  16. Kanakala, S. and Ghanim, M. 2016. RNA interference in insect vectors for plant viruses. Viruses 8:329. https://doi.org/10.3390/v8120329
  17. Karatolos, N., Williamson, M. S., Denholm, I., Gorman, K., Ffrench-Constant, R. H. and Bass, C. 2012. Over-expression of a cytochrome P450 is associated with resistance to pyriproxyfen in the greenhouse whitefly Trialeurodes vaporariorum. PLoS ONE 7:e31077. https://doi.org/10.1371/journal.pone.0031077
  18. Lamb, D. C., Lei, L., Warrilow, A. G. S., Lepesheva, G. I., Mullins, J. G. L., Waterman, M. R. and Kelly, S. L. 2009. The first virally encoded cytochrome p450. J. Virol. 83:8266-8269. https://doi.org/10.1128/JVI.00289-09
  19. Langmead, B. and Salzberg, S. L. 2012. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9:357-359. https://doi.org/10.1038/nmeth.1923
  20. Lee, J. H., Choi, J. Y., Tao, X. Y., Kim, J. S., Kim, W. and Je, Y. H. 2013. Transcriptome analysis of the small brown planthopper, Laodelphax striatellus carrying Rice stripe virus. Plant Pathol. J. 29:330-337. https://doi.org/10.5423/PPJ.NT.01.2013.0001
  21. Lee, K. S., Kim, S. R., Park, N. S., Kim, I., Kang, P. D., Sohn, B. H., Choi, K. H., Kang, S. W., Je, Y. H., Lee, S. M., Sohn, H. D. and Jin, B. R. 2005. Characterization of a silkworm thioredoxin peroxidase that is induced by external temperature stimulus and viral infection. Insect Biochem. Mol. Biol. 35:73-84. https://doi.org/10.1016/j.ibmb.2004.09.008
  22. Liu, B., Qin, F., Liu, W. and Wang, X. 2016. Differential proteomics profiling of the ova between healthy and Rice stripe virus-infected female insects of Laodelphax striatellus. Sci. Rep. 6:27216. https://doi.org/10.1038/srep27216
  23. Liu, W., Gray, S., Huo, Y., Li, L., Wei, T. and Wang, X. 2015. Proteomic analysis of interaction between a plant virus and its vector insect reveals new functions of hemipteran cuticular protein. Mol. Cell. Proteomics 14:2229-2242. https://doi.org/10.1074/mcp.M114.046763
  24. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. and Wold, B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5:621-628. https://doi.org/10.1038/nmeth.1226
  25. Ng, J. C. and Falk, B. W. 2006. Virus-vector interactions mediating nonpersistent and semipersistent transmission of plant viruses. Annu. Rev. Phytopathol. 44:183-212. https://doi.org/10.1146/annurev.phyto.44.070505.143325
  26. Patel, R. K. and Jain, M. 2012. NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS One 7:e30619. https://doi.org/10.1371/journal.pone.0030619
  27. Pinheiro, P. V., Ghanim, M., Alexander, M., Rebelo, A. R., Santos, R. S., Orsburn, B. C., Gray, S. and Cilia, M. 2017. Host plants indirectly influence plant virus transmission by altering gut cysteine protease activity of aphid vectors. Mol. Cell. Proteomics 16(4 Suppl 1):S230-S243. https://doi.org/10.1074/mcp.M116.063495
  28. Premzl, A., Turk, V. and Kos, J. 2006. Intracellular proteolytic activity of cathepsin B is associated with capillary-like tube formation by endothelial cells in vitro. J. Cell. Biochem. 97:1230-1240. https://doi.org/10.1002/jcb.20720
  29. Roberts, A. and Pachter, L. 2013. Streaming fragment assignment for real-time analysis of sequencing experiments. Nat. Methods 10:71-73. https://doi.org/10.1038/nmeth.2251
  30. Shiba, H., Uchida, D., Kobayashi, H. and Natori, M. 2001. Involvement of cathepsin B- and L-like proteinases in silk gland histolysis during metamorphosis of Bombyx mori. Arch. Biochem. Biophys. 390:28-34. https://doi.org/10.1006/abbi.2001.2343
  31. Sim, S., Ramirez, J. L. and Dimopoulos, G. 2012. Dengue virus infection of the Aedes aegypti salivary gland and chemosensory apparatus induces genes that modulate infection and blood-feeding behavior. PLoS Pathog. 8:e1002631. https://doi.org/10.1371/journal.ppat.1002631
  32. Storr, S. J., Woolston, C. M., Zhang, Y. and Martin, S. G. 2013. Redox environment, free radical, and oxidative DNA damage. Antioxid. Redox Signal. 18:2399-2408. https://doi.org/10.1089/ars.2012.4920
  33. Stram, Y. and Kuzntzova, L. 2006. Inhibition of viruses by RNA interference. Virus Genes 32:299-306. https://doi.org/10.1007/s11262-005-6914-0
  34. Toriyama, S. 1986. Rice stripe virus: prototype of a new group of viruses that replicate in plants and insects. Microbiol. Sci. 3:347-351.
  35. Van Rij, R. P., Saleh, M.-C., Berry, B., Foo, C., Houk, A., Antoniewski, C. and Andino, R. 2006. The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev. 20:2985-2995. https://doi.org/10.1101/gad.1482006
  36. Wang, X.-H., Aliyari, R., Li, W.-X., Li, H.-W., Kim, K., Carthew, R., Atkinson, P. and Ding, S.-W. 2006. RNA interference directs innate immunity against viruses in adult Drosophila. Science 312:452-454. https://doi.org/10.1126/science.1125694
  37. Wei, T.-Y., Yang, J.-G., Liao, F.-L., Gao, F.-L., Lu, L.-M., Zhang, X.-T., Li, F., Wu, Z.-J., Lin, Q.-Y., Xie, L.-H. and Lin, H.-X. 2009. Genetic diversity and population structure of rice stripe virus in China. J. Gen. Virol. 90:1025-1034. https://doi.org/10.1099/vir.0.006858-0
  38. Wu, W., Zheng, L., Chen, H., Jia, D., Li, F. and Wei, T. 2014. Nonstructural protein NS4 of Rice Stripe Virus plays a critical role in viral spread in the body of vector insects. PLoS ONE 9:e88636. https://doi.org/10.1371/journal.pone.0088636
  39. Xu, Y., Huang, L., Fu, S., Wu, J. and Zhou, X. 2012. Population diversity of rice stripe virus-derived siRNAs in three different hosts and RNAi-based antiviral immunity in Laodelphgax striatellus. PLoS ONE 7:e46238. https://doi.org/10.1371/journal.pone.0046238
  40. Yang, M., Xu, Z., Zhao, W., Liu, Q., Li, Q., Lu, L., Liu, R., Zhang, X. and Cui, F. 2018. Rice stripe virus-derived siRNAs play different regulatory roles in rice and in the insect vector Laodelphax striatellus. BMC Plant Biol. 18:219. https://doi.org/10.1186/s12870-018-1438-7
  41. Yang, X.-M., Hou, L.-J., Dong, D.-J., Shao, H.-L., Wang, J.-X. and Zhao, X.-F. 2006. Cathepsin B-like proteinase is involved in the decomposition of the adult fat body of Helicoverpa armigera. Arch. Insect Biochem. Physiol. 62:1-10. https://doi.org/10.1002/arch.20115
  42. Zhao, X.-F., An, X.-M., Wang, J.-X., Dong, D.-J., Du, X.-J., Sueda, S. and Kondo, H. 2005. Expression of the Helicoverpa cathepsin b-like proteinase during embryonic development. Arch. Insect Biochem. Physiol. 58:39-46. https://doi.org/10.1002/arch.20030
  43. Zhao, W., Lu, L., Yang, P., Cui, N., Kang, L. and Cui, F. 2016a. Organ-specific transcriptome response of the small brown planthopper toward rice stripe virus. Insect Biochem. Mol. Biol. 70:60-72. https://doi.org/10.1016/j.ibmb.2015.11.009
  44. Zhao, W., Yang, P., Kang, L. and Cui, F. 2016b. Different pathogenicities of Rice stripe virus from the insect vector and from viruliferous plants. New Phytol. 210:196-207. https://doi.org/10.1111/nph.13747
  45. Zuzarte-Luis, V., Montero, J. A., Kawakami, Y., Izpisua-Belmonte, J. C. and Hurle, J. M. 2007. Lysosomal cathepsins in embryonic programmed cell death. Dev. Biol. 301:205-217. https://doi.org/10.1016/j.ydbio.2006.08.008