The tomato spotted wilt virus genome is processed differentially in its plant host Arachis hypogaea and its thrips vector Frankliniella fusca

Frontiers in Plant Science

Volumn 7, Issue September, 2016, Pages

  Fletcher, Stephen J ^a   Shrestha, Anita ^b   Peters, Jonathan R ^a   Carroll, Bernard J ^a   Srinivasan, Rajagopalbabu ^b   Pappu, Hanu R ^c   Mitter, Neena ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF GEORGIA   (United States)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Arachis hypogea; Frankliniella fusca; Plant defense; Plant insect virus interactions; Small RNA; Tomato spotted wilt virus; vsiRNA

Indexed keywords

EID: 84988568747     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.01349     Document Type: Article

References (61)

1. Baulcombe, D. (2004). RNA silencing in plants. Nature 431, 356-363. doi: 10.1038/nature02874
2. Bolduc, F., Hoareau, C., St-Pierre, P., and Perreault, J. P. (2010). In-depth sequencing of the siRNAs associated with peach latent mosaic viroid infection. BMC Mol. Biol. 11:16. doi: 10.1186/1471-2199-11-16
3. Bologna, N. G., and Voinnet, O. (2014). The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu. Rev. Plant Biol. 65, 473-503. doi: 10.1146/annurev-arplant-050213-035728
4. Campbell, C. L., Keene, K. M., Brackney, D. E., Olson, K. E., Blair, C. D., Wilusz, J., et al. (2008). Aedes aegypti uses RNA interference in defense against Sindbis virus infection. BMC Microbiol. 8:47. doi: 10.1186/1471-2180-8-47
5. Culbreath, A. K., and Srinivasan, R. (2011). Epidemiology of spotted wilt disease of peanut caused by Tomato spotted wilt virus in the southeastern U.S. Virus Res. 159, 101-109. doi: 10.1016/j.virusres.2011.04.014
6. Dash, S., Cannon, E. K. S., Kalberer, S. R., Farmer, A. D., and Cannon, S. B. (2016). "Chapter 8 - peanutbase and other bioinformatic resources for peanut A2," in Peanuts eds R. F. Wilson and H. T. Stalker (Urbana IL: AOCS Press) 241-252.
7. Dehaan, P., Kormelink, R., Resende, R. D., Vanpoelwijk, F., Peters, D., and Goldbach, R. (1991). Tomato spotted wilt virus-L RNA encodes a putative RNA-polymerase. J. Gen. Virol. 72,2207-2216.doi: 10.1099/0022-1317-72-9-2207
8. Dehaan, P., Wagemakers, L., Peters, D., and Goldbach, R. (1990). The S-RNA segment of Tomato spotted wilt virus has an ambisense character. J. Gen. Virol. 71,1001-1007. doi: 10.1099/0022-1317-71-5-1001
9. Ding, S.-W., and Voinnet, O. (2007). Antiviral immunity directed by small RNAs. Cell 130, 413-426. doi: 10.1016/j.cell.2007.07.039
10. Ding, S. W. (2010). RNA-based antiviral immunity. Nat. Rev. Immunol. 10, 632644. doi: 10.1038/nri2824
11. Donaire, L., Barajas, D., Martinez-Garcia, B., Martinez-Priego, L., Pagan, I., and Llave, C. (2008). Structural and genetic requirements for the biogenesis of tobacco rattle virus-derived small interfering RNAs. J. Virol. 82, 5167-5177. doi: 10.1128/JVI.00272-08
12. Fletcher, S.J. (2016).SmallComplementaryRnAMapper:AQuickandSimpleSmall RNA Read Analysis Package [Online]. Available: http://carroll-lab.github.io/scram/
13. Gasciolli, V., Mallory, A. C., Bartel, D. P., and Vaucheret, H. (2005). Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr. Biol. 15, 1494-1500. doi: 10.1016/j.cub.2005.07.024
14. Groszmann, M., Greaves, I. K., Albertyn, Z. I., Scofield, G. N., Peacock, W. J., and Dennis, E. S. (2011). Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor. Proc. Natl. Acad. Sci. U.S.A. 108, 2617-2622.doi: 10.1073/pnas.1019217108
15. Harris, C. J., Molnar, A., Muller, S. Y., and Baulcombe, D. C. (2015). FDF-PAGE: a powerful technique revealing previously undetected small RNAs sequestered by complementary transcripts. Nucleic Acids Res. 43, 7590-7599. doi: 10.1093/nar/gkv604
16. Henderson, I. R., Zhang, X., Lu, C., Johnson, L., Meyers, B. C., Green, P. J., et al. (2006). Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nat. Genet. 38, 721-725.doi: 10.1038/ng1804
17. Hess, A. M., Prasad, A. N., Ptitsyn, A., Ebel, G. D., Olson, K. E., Barbacioru, C., et al. (2011). Small RNA profiling of Dengue virus-mosquito interactions implicates the PIWI RNA pathway in anti-viral defense. BMC Microbiol. 11:45. doi: 10.1186/1471-2180-11-45
18. Hong, W., Qian, D., Sun, R. H., Jiang, L., Wang, Y., Wei, C. H., et al. (2015). OsRDR6 plays role in host defense against double-stranded RNA virus, Rice Dwarf Phytoreovirus. Sci. Rep. 5,11324.doi: 10.1038/srep11324
19. Jagadeeswaran, G., Zheng, Y., Sumathipala, N., Jiang, H., Arrese, E. L., Soulages, J. L., et al. (2010). Deep sequencing of small RNA libraries reveals dynamic regulation of conserved and novel microRNAs and microRNA-stars during silk worm development. BMC Genomics 11:52. doi: 10.1186/1471-2164-11-52
20. Jia, Y., Lisch, D. R., Ohtsu, K., Scanlon, M. J., Nettleton, D., and Schnable, P. S. (2009). Loss of RNA-dependent RNA polymerase 2 (RDR2) function causes widespread and unexpected changes in the expression of transposons, genes, and 24-nt small RNAs. PLoS Genet. 5:e1000737. doi: 10.1371/journal.pgen.1000737
21. Johnson, L. M., Du, J., Hale, C. J., Bischof, S., Feng, S., Chodavarapu, R. K., et al. (2014). SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature 507, 124-128. doi: 10.1038/nature12931
22. Jones, D. R. (2005). Plant viruses transmitted by thrips. Eur. J. Plant Pathol. 113, 119-157.doi: 10.1007/s10658-005-2334-1
23. Keene, K. M., Foy, B. D., Sanchez-Vargas, I., Beaty, B. J., Blair, C. D., and Olson, K. E. (2004). RNA interference acts as a natural antiviral response to O'nyong-nyong virus (Alphavirus; Togaviridae) infection of Anopheles gambiae. Proc. Natl. Acad. Sci. U.S.A. 101, 17240-17245.doi: 10.1073/pnas.0406983101
24. Kemp, C., Mueller, S., Goto, A., Barbier, V., Paro, S., Bonnay, F., et al. (2013). Broad RNA interference-mediated antiviral immunity and virus-specific inducible responses in Drosophila. J. Immunol. 190, 650-658. doi: 10.4049/jimmunol.1102486
25. Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., et al. (2009). Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639-1645.doi: 10.1101/gr.092759.109
26. Lebas, B.S. M., and Ochoa-Corona, F. M. (2007). "Impatiens necrotic spot virus," in Characterization, Diagnosis and Management of Plant Viruses, Grain Crops and Ornamentals, Vol. 4, eds G. P. B. Rao, C. Bragard, and B. S. M. Lebas (Houston, TX: Stadium Press LLC), 221-243.
27. Lin, K. Y., Cheng, C. P., Chang, B. C., Wang, W. C., Huang, Y. W., Lee, Y. S., et al. Global analyses of small interfering RNAs derived from Bamboo mosaic virus and its associated satellite RNAs in different plants. PLoS ONE 5:e11928. doi: 10.1371/journal.pone.0011928
28. Mallory, A. C., and Vaucheret, H. (2004). MicroRNAs: something important between the genes. Curr. Opin. Plant Biol. 7, 120-125. doi: 10.1016/j.pbi.2004.01.006
29. Mandal, S. K. (2012). Field evaluation of alternate use of insecticides against chilli thrips, Scirtothrips dorsalis (Hood). Ann. Plant Protect. Sci. 20, 59-62.
30. Margaria, P., Bosco, L., Vallino, M., Ciuffo, M., Mautino, G. C., Tavella, L., et al. (2014). The NSs protein of tomato spotted wilt virus is required for persistent infection and transmission byFrankliniella occidentalis. J. Virol. 88, 5788-5802. doi: 10.1128/JVI.00079-14
31. Margaria, P., Miozzi, L., Rosa, C., Axtell, M. J., Pappu, H. R., and Turina, M. (2015). Small RNA profiles of wild-type and silencing suppressor-deficient tomato spotted wilt virus infected Nicotiana benthamiana. Virus Res. 208, 30-38. doi: 10.1016/j.virusres.2015.05.021
32. McHale, M., Eamens, A.L., Finnegan, E.J., and Waterhouse, P.M. (2013).A22-nt artificial microRNA mediates widespread RNA silencing in Arabidopsis. Plant J. 76, 519-529. doi: 10.1111/tpj.12306
33. Miozzi, L., Gambino, G., Burgyan, J., and Pantaleo, V. (2013). Genome-wide identification of viral and host transcripts targeted by viral siRNAs in Vitis vinifera. Mol. Plant Pathol. 14,30-43.doi: 10.1111/j.1364-3703.2012.00828.x
34. Mitter, N., Koundal, V., Williams, S., and Pappu, H. (2013). Differential expression of Tomato spotted wilt virus-derived viral small RNAs in infected commercial and experimental host plants. PLoS ONE 8:e76276. doi: 10.1371/journal.pone.0076276
35. Mueller, S., Gausson, V., Vodovar, N., Deddouche, S., Troxler, L., Perot, J., et al. (2010). RNAi-mediated immunity provides strong protection against the negative-strand RNA vesicular stomatitis virus in Drosophila. Proc. Nat. Acad. Sci. U.S.A. 107,19390-19395.doi: 10.1073/pnas.1014378107
36. Munger, F. (1942). A method for rearing citrus thrips in the laboratory. J. Econ. Entomol. 35, 373-375. doi: 10.1093/jee/35.3.373
37. Myles, K. M., Wiley, M. R., Morazzani, E. M., and Adelman, Z. N. (2008). Alphavirus-derived small RNAs modulate pathogenesis in disease vector mosquitoes. Proc. Nat. Acad. Sci. U.S.A. 105, 19938-19943. doi: 10.1073/pnas.0803408105
38. Pappu, H. R., Jones, R. A., and Jain, R. K. (2009). Global status of tospovirus epidemics in diverse cropping systems: successes achieved and challenges ahead. Virus Res. 141, 219-236. doi: 10.1016/j.virusres.2009.01.009
39. Parent, J. S., Bouteiller, N., Elmayan, T., and Vaucheret, H. (2015). Respective contributions of Arabidopsis DCL2 and DCL4 to RNA silencing. Plant J. 81, 223-232. doi: 10.1111/tpj.12720
40. Pelaez, P., and Sanchez, F. (2013). Small RNAs in plant defense responses during viral and bacterial interactions: similarities and differences. Front. Plant Sci. 4:343. doi: 10.3389/fpls.2013.00343
41. Persley, D. M., Thomas, J. E., and Sharman, M. (2006). Tospoviruses: an Australian perspective.Austral. PlantPathol. 35,161-180.doi: 10.1071/AP06015
42. Pontes, O., Li, C.F., Costa Nunes, P., Haag, J., Ream, T., Vitins, A., et al. (2006).The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNAprocessingcenter. Cell 126,79-92. doi: 10.1016/j.cell.2006.05.031
43. Riley, D. G., Joseph, S. V., Srinivasan, R., and Diffie, S. (2011). Thrips vectors of tospoviruses. J. Int. Pest Manag. 1, 1-10.
44. Rotenberg, D., Krishna Kumar, N. K., Ullman, D. E., Montero-Astua, M., Willis, D. K., German, T. L., et al. (2009). Variation in tomato spotted wilt virus titer in Frankliniella occidentalis and its association with frequency of transmission. Phytopathology 99, 404-410.doi: 10.1094/PHYTO-99-4-0404
45. Schnettler, E., Hemmes, H., Huismann, R., Goldbach, R., Prins, M., and Kormelink, R. (2010). Diverging affinity of tospovirus RNA silencing suppressor proteins, NSs, for various RNA duplex molecules. J. Virol. 84, 11542-11554. doi: 10.1128/JVI.00595-10
46. Scholthof, K. B., Adkins, S., Czosnek, H., Palukaitis, P., Jacquot, E., Hohn, T., et al. Top 10 plant viruses in molecular plant pathology. Mol. Plant Pathol. 12, 938-954. doi: 10.1111/j.1364-3703.2011.00752.x
47. Silva, T. F., Romanel, E. A. C., Andrade, R. R. S., Farinelli, L., Osteras, M., Deluen, C., et al. (2011). Profile of small interfering RNAs from cotton plants infected with the polerovirus Cotton leafroll dwarf virus. BMC Mol. Biol. 12:40. doi: 10.1186/1471-2199-12-40
48. Smith, N. A., Eamens, A. L., and Wang, M. B. (2010). The presence of high-molecular-weight viral RNAs interferes with the detection of viral small RNAs. RNA 16, 1062-1067. doi: 10.1261/rna.2049510
49. Snippe, M., Smeenk, L., Goldbach, R., and Kormelink, R. (2007). The cytoplasmic domain of tomato spotted wilt virus Gn glycoprotein is required for Golgi localisation and interaction with Gc. Virology 363, 272-279. doi: 10.1016/j.virol.2006.12.038
50. Soellick, T. R., Uhrig, J. F., Bucher, G. L., Kellmann, J. W., and Schreier, P. H. (2000).ThemovementproteinNSmoftomatospottedwilttospovirus(TSWV): RNA binding, interaction with the TSWV N protein, and identification of interacting plant proteins. Proc. Nat. Acad. Sci. U.S.A. 97, 2373-2378. doi: 10.1073/pnas.030548397
51. Szittya, G., Moxon, S., Pantaleo, V., Toth, G., Pilcher, R. L. R., Moulton, V., et al. (2010). Structural and functional analysis of viral siRNAs. PLoS Pathog. 6:e1000838. doi: 10.1371/journal.ppat.1000838
52. Takeda, A., Sugiyama, K., Nagano, H., Mori, M., Kaido, M., Mise, K., et al. (2002). Identification of a novel RNA silencing suppressor, NSs protein of Tomato spotted wilt virus. FEBS Lett. 532, 75-79.
53. Tsompana, M., and Moyer, J. W. (2008). "Tospoviruses," in Encyclopedia of Virology, 3rd Edn, eds B. W. J. Mahy and M. H. V. Van Regenmortel (Oxford: Elsevier Ltd), 157-162.
54. Ullman, D. E., German, T. L., Sherwood, J. L., Westcot, D. M., and Cantone, F. A. (1993). Tospovirus replication in insect vector cells - immunocytochemical evidence that the nonstructural protein encoded by the S-RNA of Tomato spotted wilt tospovirus is present in thrips vector cells. Phytopathology 83, 456-463. doi: 10.1094/Phyto-83-456
55. Wang, X. B., Wu, Q. F., Ito, T., Cillo, F., Li, W. X., Chen, X. M., et al. (2010). RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. Proc. Nat. Acad. Sci. U.S.A. 107, 484-489. doi: 10.1073/pnas.0904086107
56. Wei, Y., Chen, S., Yang, P., Ma, Z., and Kang, L. (2009). Characterization and comparative profiling of the small RNA transcriptomes in two phases of locust. Genome Biol. 10, R6. doi: 10.1186/gb-2009-10-1-r6
57. Whitfield, A. E., Ullman, D. E., and German, T. L. (2005). Tospovirus-thrips interactions. Annu. Rev. Phytopathol. 43, 459-489. doi: 10.1146/annurev.phyto.43.040204.140017
58. Wierzbicki, A. T., Ream, T. S., Haag, J. R., and Pikaard, C. S. (2009). RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat. Genet. 41, 630-634. doi: 10.1038/ng.365
59. Wu, Q. F., Luo, Y. J., Lu, R., Lau, N., Lai, E. C., Li, W. X., et al. (2010). Virus discovery by deep sequencing and assembly of virus-derived small silencing RNAs. Proc. Nat. Acad. Sci. U.S.A. 107, 1606-1611. doi: 10.1073/pnas.0911353107
60. 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 Laodelphax striatellus. PLoS ONE 7:e46238. doi: 10.1371/journal.pone.0046238
61. Zhang, C., Wu, Z., Li, Y., and Wu, J. (2015). Biogenesis, function, and applications of virus-derived Small RNAs in plants. Front. Microbiol. 6:1237. doi: 10.3389/fmicb.2015.01237