Transgenic strategies to confer resistance against viruses in rice plants

Frontiers in Microbiology

Volumn 4, Issue JAN, 2013, Pages

  Sasaya, Takahide ^a   Nakazono Nagaoka, Eiko ^b   Saika, Hiroaki ^c   Aoki, Hideyuki ^d   Hiraguri, Akihiro ^e   Netsu, Osamu ^e   Uehara Ichiki, Tamaki ^c   Onuki, Masatoshi ^a   Toki, Seichi ^c   Saito, Koji ^d   Yatou, Osamu ^d  

^a NATIONAL AGRICULTURAL RESEARCH CENTER FOR KYUSHU OKINAWA REGION   (Japan)

^b NATIONAL INSTITUTE OF FRUIT TREE SCIENCE   (Japan)

^c NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^d FOOD RESEARCH INSTITUTE   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

Author keywords

Forage rice cultivar; Reoviridae; RNA interference; Tenuivirus; Transgenic rice

Indexed keywords

CAP BINDING PROTEIN; PLANT VIRUS MOVEMENT PROTEIN; RNA DIRECTED RNA POLYMERASE; RNA INDUCED SILENCING COMPLEX; VIRUS RNA;

AMINO ACID SEQUENCE; CULTIVAR; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC RESISTANCE; GENETIC SIMILARITY; GENETIC TRANSFORMATION; GENOME ANALYSIS; NONHUMAN; PLANT VIRUS; POSTTRANSCRIPTIONAL GENE SILENCING; REOVIRUS; REVIEW; RICE GALL DWARF VIRUS; RICE GRASSY STUNT VIRUS; RICE HOJA BLANCA VIRUS; RNA INTERFERENCE; RNA VIRUS INFECTION; SEQUENCE ANALYSIS; TENUIVIRUS; TRANSGENIC PLANT; VIRUS CAPSID; VIRUS INHIBITION;

EID: 84893643729     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2013.00409     Document Type: Review

References (98)

1. Akita, F., Miyazaki, N., Hibino, H., Shimizu, T., Higashiura, A., Uehara-Ichiki, T., et al. (2011). Viroplasm matrix protein Pns9 from rice gall dwarf virus forms an octameric cylindrical structure. J. Gen. Virol. 92, 2214-2221. doi: 10.1099/vir.0.032524-0
2. Attoui, H., Mertens, P. P. C., Becnel, J., Belaganahalli, S., Bergoin, M., Brussaard, C. P., et al. (2011). "Family reoviridae," in Virus Taxonomy: Classification and Nomenclature, Ninth Report of the International Commitee on Taxonomy of Viruses, eds A. M. Q. King, M. J. Adams, E. B. Carstens, and E. J. Lefkowitz (San Diego, CA: Academic Press), 541-637.
3. Azzam, O., and Chancellor, T. C. B. (2002). The biology, epidemiology, and management of rice tungro disease in Asia. Plant Dis. 86, 88-100. doi: 10.1094/PDIS.2002.86.2.88
4. Bau, H. J., Cheng, Y. H., Yu, T. A., Yang, J. S., and Yeh, S. D. (2003). Broad-spectrum resistance to different geographic strains of Papaya ringspot virus in coat protein gene transgenic papaya. Phytopathology 93, 112-120. doi: 10.1094/PHYTO.2003.93.1.112
5. Baulcombe, D. (1996). Mechanisms of pathogen-derived resistance to viruses in transgenic plants. Plant Cell 8, 1833-1844. doi: 10.1105/tpc.8.10.1833
6. Baulcombe, D. (2004). RNA silencing in plants. Nature 431, 356-363. doi: 10.1038/nature02874
7. Baulcombe, D. (2005). RNA silencing. Trends Biochem. Sci. 30, 290-293. doi: 10.1016/j.tibs.2005.04.012
8. Bernstein, E., Caudy, A., Hammond, S., and Hannon G. (2001). Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363-366. doi: 10.1038/35053110
9. Bonfim, K., Faria, J. C., Nogueira, E. O. P. L., Mendes, É. A., and Aragão, F. J. L. (2007). RNAi-mediated resistance to Bean golden mosaic virus in genetically engineered common bean (Phaseolus vulgaris). Mol. Plant Microbe Interact. 20, 717-726. doi: 10.1094/MPMI-20-6-0717
10. Brigneti, G., Voinnet, O., Li, W. X., Ji, L. H., Ding, S. W., and Baulcombe, D. C. (1998). Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J. 17, 6739-6746. doi: 10.1093/emboj/17.22.6739
11. Brogdon, W. G., and McAllister, J. C. (1998). Insecticide resistance and vector control. Emerg. Infect. Dis. 4, 605-613. doi: 10.3201/eid0404.980410
12. Bucher, E., Lohuis, D., van Poppel, P. M. J. A., Geerts-Dimitriadou, C., Goldbach, R., and Prins, M. (2006). Multiple virus resistance at a high frequency using a single transgene construct. J. Gen. Virol. 87, 3697-3701. doi: 10.1099/vir.0.82276-0
13. Bucher, E., Sijen, T., de Haan, P., Goldbach, R., and Prins, M. (2003). Negative-strand tospoviruses and tenuiviruses carry a gene for a suppressor of gene silencing at analogous genomic positions. J. Virol. 77, 1329-1336. doi: 10.1128/JVI.77.2.1329-1336.2003
14. Cabauatan, P. Q., Cabunagan, R. C., and Choi., I.-R. (2009). "Rice viruses transmitted by the brown planthopper Nilaparvata lugens Stål," in Planthoppers: New Threats to the Sustainability of Intensive Rice Production Systems in Asia eds (K. L. Heong and B. Hardy) PA, Los Baños; IRRI, 357-358.
15. Cao, X., Zhou, P., Zhang, X., Zhu, S., Zhong, X., Xiao, Q., et al. (2005). Identification of an RNA silencing suppressor from a plant double-stranded RNA virus. J. Virol. 79, 13018-13027. doi: 10.1128/JVI.79.20.13018-13027.2005
16. de Miranda, J., Hernandez, M., Hull, R., and Espinoza, A. M. (1994). Sequence analysis of rice hoja blanca virus RNA 3. J. Gen. Virol. 75, 2127-2132. doi: 10.1099/0022-1317-75-8-2127
17. 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
18. Dunoyer, P., Pfeffer, S., Fritsch, C., Hemmer, O., Voinnet, O., and Richards, K. E. (2002). Identification, subcellular localization and some properties of a cysteine-rich suppressor of gene silencing encoded by peanut clump virus. Plant J. 29, 555-567. doi: 10.1046/j.0960-7412.2001.01242.x
19. Eaton, B. T., Hyatt, A. D., and White, J. R. (1987). Association of bluetongue virus with the cytoskeleton. Virology 157, 107-116. doi: 10.1016/0042-6822(87)90319-9
20. Falk, B. W., Morales, F. J., Tsai, J. H., and Niessen, A. I. (1987). Serological and biochemical properties of the capsid and major noncapsid proteins of maize stripe, rice hoja blanca, and Echinochloa hoja blanca viruses. Phytopathology 77, 196-201. doi: 10.1094/Phyto-77-196
21. Falk, B. W., and Tsai, J. H. (1998). Biology and molecular biology of viruses in the genus Tenuivirus. Annu. Rev. Phytopathol. 36, 139-163. doi: 10.1146/annurev.phyto.36.1.139
22. Fusaro, A., Matthew, L., Smith, N., Curtin, S., Dedic-Hagan, J., Ellacott, G., et al. (2006). RNA interference-inducing hairpin RNAs in plants act through the viral defence pathway. EMBO Rep. 7, 1168-1175. doi: 10.1038/sj.embor.7400837
23. Hassani-Mehraban, A., Brenkman, A. B., van den Broek, N. J. F., Goldbach, R., and Kormelink, R. (2009). RNAi-mediated transgenic Tospovirus resistance broken by intraspecies silencing suppressor protein complementation. Mol. Plant Microbe Interact. 22, 1250-1257. doi: 10.1094/MPMI-22-10-1250
24. Hayano, Y., Kakutani, T., Hayashi, T., and Minobe, Y. (1990). Coding strategy of Rice stripe virus: major nonstructural protein is encoded in viral RNA segment 4 and coat protein in RNA complementary to segment 3. Virology 177, 372-374. doi: 10.1016/0042-6822(90)90493-B
25. Hemmes, H., Lakatos, L., Goldbach, R., Burgyán, J., and Prins, M. (2007). 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, 1079-1089. doi: 10.1261/rna.444007
26. Hibino, H. (1996). Biology and epidemiology of rice viruses. Annu. Rev. Phytopathol. 34, 249-274. doi: 10.1146/annurev.phyto.34.1.249
27. Hiraguri, A., Netsu, O., Shimizu, T., Uehara-Ichiki, T., Omura, T., Sasaki, N., et al. (2011). The nonstructural protein pC6 of rice grassy stunt virus trans-complements the cell-to-cell spread of a movement-defective tomato mosaic virus. Arch. Virol. 156, 911-916. doi: 10.1007/s00705-011-0939-6
28. Hiraguri, A., Ueki, S., Kondo, H., Nomiyama, K., Shimizu, T., Ichiki-Uehara, T., et al. (2013). Identification of a movement protein of Mirafiori lettuce big-vein ophiovirus. J. Gen. Virol. 94, 1145-1150. doi: 10.1099/vir.0.050005-0
29. Hoang, A. T., Zhang, H. M., Yang, J., Chen, J. P., Hébrard, E., Zhou, G. H., et al. (2011). Identification, characterization, and distribution of southern rice black-streaked dwarf virus in Vietnam. Plant Dis. 95, 1063-1069. doi: 10.1094/PDIS-07-10-0535
30. Ishii, M., and Yoshimura, S. (1973). Epidemiological studies on rice black-streaked dwarf virus in Kanto-Tosan district in Japan. J. Cent. Agric. Exp. Stat. 17, 61-121.
31. Isogai, M., Uyeda, I., and Lee, B. (1998). Detection and assignment of proteins encoded by rice black streaked dwarf fijivirus S7, S8, S9 and S10. J. Gen. Virol. 79, 1487-1494.
32. Jones, A. L., Johansen, I. E., Bean, S. J., Bach, I., and Maule, A. J. (1998). Specificity of resistance to pea seed-borne mosaic potyvirus in transgenic peas expressing the viral replicase (Nib) gene. J. Gen. Virol. 79, 3129-3137.
33. Kakutani, T., Hayano, Y., Hayashi, T., and Minobe, Y. (1990). Ambisense segment 4 of rice stripe virus: possible evolutionary relationship with phleboviruses and uukuviruses (Bunyaviridae). J. Gen. Virol. 71, 1427-1432. doi: 10.1099/0022-1317-71-7-1427
34. Kalantidis, K., Psaradakis, S., Tabler, M., and Tsagris, M. (2002). The occurrence of CMV-specific short RNAs in transgenic tobacco expressing virus-derived double-stranded RNA is indicative of resistance to the virus. Mol. Plant Microbe Interact. 15, 826-833. doi: 10.1094/MPMI.2002.15.8.826
35. Kishimoto, R. (1971). Long distance migration of plant hopper, Sogatella furcifera and Nilaparvata lugens. Trop. Agric. Res. Ser. 5, 201-216. 25.
36. Koganezawa, H. (1977). Purification and properties of rice stripe virus. Trop. Agric. Res. Ser. 10, 151-154.
37. Li, C., Song, J., and Jiang, L. (1999). Research progress on the maize rough dwarf virus disease. Plant Protect. 25, 34-37.
38. Li, Y., Bao, Y. M., Wei, C. H., Kang, Z. S., Zhong, Y. W., Mao, P., et al. (2004). Rice dwarf phytoreovirus segment S6-encoded nonstructural protein has a cell-to-cell movement function. J. Virol. 78, 5382-5389. doi: 10.1128/JVI.78.10.5382-5389.2004
39. Liu, F. X., Zhao, Q., Ruan, X. L., He, Y. W., and Li, H. P. (2008). Suppressor of RNA silencing encoded by rice gall dwarf virus genome segment 11. Chin. Sci. Bull. 53, 362-369. doi: 10.1007/s11434-008-0095-x
40. Lucas, W. J. (2006). Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344, 169-184. doi: 10.1016/j.virol.2005.09.026
41. Mao, Q., Zheng, S., Han, Q., Chen, H., Ma, Y., Jia, D., et al. (2013). New model for the genesis and maturation of viroplasms induced by Fijiviruses in insect vector cells. J. Virol. 87, 6819-6828. doi: 10.1128/JVI.00409-13
42. Mendoza, E. M. T., Laurena, A. C., and Botella, J. R. (2008). Recent advances in the development of transgenic papaya technology. Biotechnol. Annu. Rev. 14, 423-462. doi: 10.1016/S1387-2656(08)00019-7
43. McNulty, M. S., Curran, W. L., and McFerran, J. B. (1976). The morphogenesis of a cytopathic bovine rotavirus in Madin-Darby bovine kidney cells. J. Gen. Virol. 33, 503-508. doi: 10.1099/0022-1317-33-3-503
44. Miller, E. D., and Hemenway, C. (1998). History of coat protein mediated protection. Methods Mol. Biol. 81, 25-38.
45. Miranda, G. J., and Koganezawa, H. (1995). Identification, purification, and serological detection of the major noncapsid protein of rice grassy stunt virus. Phytopathology 85, 1530-1533. doi: 10.1094/Phyto-85-1530
46. Morozov, S. Y., and Solovyev, A. G. (2003). Triple gene block: modular design of a multifunctional machine for plant virus movement. J. Gen. Virol. 84, 1351-1366. doi: 10.1099/vir.0.18922-0
47. Nguyen, M., Ramirez, B.-C., Goldbach, R., and Haenni, A.-L. (1997). Characterization of the in vitro activity of the RNA-dependent RNA polymerase associated with the ribonucleoproteins of Rice hoja blanca Tenuivirus. J. Virol. 71, 2621-2627.
48. Noda, S., Omura, T., Murakami, M., and Tsuchizaki, T. (1991). Infectivity of rice viruses to the varieties resistant to rice stripe virus. Ann. Phytopathol. Soc. Jpn. 57, 259-262. doi: 10.3186/jjphytopath.57.259
49. Normile, D. (2008). Reinventing rice to feed the world. Science 321, 330-337. doi: 10.1126/science.321.5887.330
50. Omura, T., and Yan, J. (1999). Role of outer capsid proteins in transmission of Phytoreovirus by insect vectors. Adv. Virus Res. 54, 15-43. doi: 10.1016/S0065-3527(08)60364-4
51. Palukaitis, P., and Zaitlin, M. (1997). Replicase-mediated resistance to plant virus disease. Adv. Virus Res. 48, 349-377. doi: 10.1016/S0065-3527(08)60292-4
52. Pfeffer, S., Dunoyer, P., Heim, F., Richards, K. E., Jonard, G., and Ziegler-Graff, V. (2002). P0 of beet Western yellows virus is a suppressor of posttranscriptional gene silencing. J. Virol. 76, 6815-6824. doi: 10.1128/JVI.76.13.6815-6824.2002
53. Pruss, G., Ge, X., Shi, X. M., Carrington, J. C., and Bowman Vance, V. (1997). Plant viral synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 9, 859-868. doi: 10.1105/tpc.9.6.859
54. Pu, Y., Kikuchi, A., Moriyasu, Y., Tomaru, M., Jin, Y., Suga, H., et al. (2011). Rice dwarf viruses with dysfunctional genomes generated in plants are filtered out in vector insects: implications for the origin of the virus. J. Virol. 85, 2975-2979. doi: 10.1128/JVI.02147-10
55. Ramirez, B. C., Garcin, D., Calvert, L. A., Kolakofsky, D., and Haenni, A.-L. (1995). Capped nonviral sequences at the 5′ end of the mRNAs of Rice hoja blanca virus RNA4. J. Virol. 69, 1951-1954.
56. Sasaya, T., Aoki, H., Omura, T., Yatou, O., and Saito, K. (2013). Development of virus-resistant transgenic forage rice cultivars. AFFRIC Res. Ser. 510, 15-18.
57. Sanford, J. C., and Johnston, S. A. (1985). The concept of parasite-derived resistance-driving resistance genes from the parasite's own genome. J. Theor. Biol. 113, 395-405. doi: 10.1016/S0022-5193(85)80234-4
58. Schnettler, E., Hemmes, H., Goldbach, R., and Prins, M. (2008). The NS3 protein of rice hoja blanca virus suppresses RNA silencing in mammalian cells. J. Gen. Virol. 89, 336-340. doi: 10.1099/vir.0.83293-0
59. Scholthof, H. B. (2005). Plant virus transport: motions of functional equivalence. Trends Plant Sci. 10, 376-382. doi: 10.1016/j.tplants.2005.07.002
60. Sharpe, A. H., Chen, L. B., and Fields, B. N. (1982). The interaction of mammalian reoviruses with the cytoskeleton of monkey kidney CV-1 cells. Virology 120, 399-411. doi: 10.1016/0042-6822(82)90040-X
61. Shiba, T. (2012). "Re-emergence of rice stripe disease and its insect vector, the small brown planthopper, in Kanto region," in Proceedings of NARO International Symposium 2012. (Fukuoka: NARO), 4.
62. Shimizu, T., Nakazono-Nagaoka, E., Akita, F., Uehara-Ichiki, T., Omura, T., and Sasaya, T. (2011a). Immunity to Rice black streaked dwarf virus, a plant reovirus, can be achieved in rice plants by RNA silencing against the gene for the viroplasm matrix protein. Virus Res. 160, 400-403. doi: 10.1016/j.virusres.2011.05.011
63. Shimizu, T., Nakazono-Nagaoka, E., Uehara-Ichiki, T., Sasaya, T., and Omura, T. (2011b). Targeting specific genes for RNA interference is crucial to the development of strong resistance to Rice stripe virus. Plant Biotechnol. J. 9, 503-512. doi: 10.1111/j.1467-7652.2010.00571.x
64. Shimizu, T., Nakazono-Nagaoka, E., Akita, F., Wei, T., Sasaya, T., Omura, T., et al. (2012). Hairpin RNA derived from the gene for Pns9, a viroplasm matrix protein of Rice gall dwarf virus, confers strong resistance to virus infection in transgenic rice plants. J. Biotechnol. 157, 421-427. doi: 10.1016/j.jbiotec.2011.12.015
65. Shimizu, T., Ogamino, T., Hiraguri, A., Nakazono-Nagaoka, E., Uehara-Ichiki, T., Nakajima, M., et al. (2013). Strong resistance against Rice grassy stunt virus is induced in transgenic rice plants expressing dsRNA of the viral genes for nucleocapsid or movement proteins as targets for RNA interference. Phytopathology 103, 513-519. doi: 10.1094/PHYTO-07-12-0165-R
66. Shimizu, T., Toriyama, S., Takahashi, M., Akutsu, K., and Yoneyama, K. (1996). Non-viral sequences at the 5′ termini of mRNAs derived from virus-sense and virus-complementary sequences of the ambisense RNA segments of rice stripe Tenuivirus. J. Gen. Virol. 77, 541-546. doi: 10.1099/0022-1317-77-3-541
67. Shimizu, T., Yoshii, M., Wei, T., Hirochika, H., and Omura, T. (2009). Silencing by RNAi of the gene for Pns12, a viroplasm matrix protein of Rice dwarf virus, results in strong resistance of transgenic rice plants to the virus. Plant Biotechnol. J. 7, 24-32. doi: 10.1111/j.1467-7652.2008.00366.x
68. Shirako, Y., Falk, B. W., and Haenni, A.-L. (2011). "Genus Tenuivirus," in Virus Taxonomy: Classification and Nomenclature. Ninth Report of the International Commitee on Taxonomy of Viruses, eds A. M. Q. King, M. J. Adams, E. B. Carstens, and E. J. Lefkowitz (San Diego, CA: Academic Press), 771-776.
69. Suzuki, N. (1993). In vitro translation of rice dwarf phytoreovirus genome segments S4 to S10. Arch. Virol. 130, 201-208. doi: 10.1007/BF01319009
70. Suzuki, N., Harada, M., and Kusano, T. (1991). Molecular analysis of rice dwarf phytoreovirus segment S11 corresponding to wound tumour phytoreovirus segment S12. J. Gen. Virol. 72, 2233-2237. doi: 10.1099/0022-1317-72-9-2233
71. Suzuki, N., Tanimura, M., Watanabe, Y., Kusano, T., Kitagawa, Y., Suda, N., et al. (1992a). Molecular analysis of rice dwarf phytoreovirus segment S1: interviral homology of the putative RNA-dependent RNA polymerase between plant- and animal-infecting reoviruses. Virology 190, 240-247. doi: 10.1016/0042-6822(92)91210-L
72. Suzuki, N., Sugawara, M., and Kusano, T. (1992b). Rice dwarf phytoreovirus segment S12 transcript ls tricistronic in vitro. Virology 191, 992-995. doi: 10.1016/0042-6822(92)90279-X
73. Suzuki, N., Watanabe, Y., Kusano, T., and Kitagawa, Y. (1990a). Sequence analysis of the rice dwarf phytoreovirus segment S3 transcript encoding for the major structural core protein of 114 kDa. Virology 179, 455-459. doi: 10.1016/0042-6822(90)90314-H
74. Suzuki, N., Watanabe, Y., Kusano, T., and Kitagawa, Y. (1990b). Sequence analysis of rice dwarf phytoreovirus genome segments S4, S5, and S6: comparison with the equivalent wound tumor virus segments. Virology 179, 446-454. doi: 10.1016/0042-6822(90)90313-G
75. Taliansky, M., Torrance, L., and Kalinina, N. O. (2008). Role of plant virus movement proteins. Methods Mol. Biol. 451, 33-54. doi: 10.1007/978-1-59745-102-4_3
76. Takahashi, M., Toriyama, S., Hamamatsu, C., and Ishihama, A. (1993). Nucleotide sequence and possible ambisense coding strategy of rice stripe virus RNA segment 2. J. Gen. Virol. 74, 769-773. doi: 10.1099/0022-1317-74-4-769
77. Toriyama, S. (ed.). (2010). Rice Stripe: A Serious Threat to Rice Crops of Japan. Tokyo: Soufusha Press, 1-306.
78. Toriyama, S. (1986). An RNA-dependent RNA polymerase associated with the filamentous nucleoproteins of Rice stripe virus. J. Gen. Virol. 67, 1247-1255. doi: 10.1099/0022-1317-67-7-1247
79. Toriyama, S., Kimishima, T., and Takahashi, M. (1997). The proteins encoded by rice grassy stunt virus RNA5 and RNA6 are only distantly related to the corresponding proteins of other members of the genus Tenuivirus. J. Gen. Virol. 78, 2355-2363.
80. Toriyama, S., Kimishima, T., Takahashi, M., Shimizu, T., Minaka, N., and Ishihama, A. (1994). Nucleotide sequence of RNA1, the largest genomic segment of rice stripe virus, the prototype of the tenuiviruses. J. Gen. Virol. 75, 3569-3579. doi: 10.1099/0022-1317-75-12-3569
81. Toriyama, S., Takahashi, M., Sano, Y., Shimizu, T., and Akutsu, K. (1998). The complete nucleotide sequence of the rice grassy stunt virus genome and genomic comparisons with viruses of the genus Tenuivirus. J. Gen. Virol. 79, 2051-2058.
82. Touris-Otero, F., Martínez-Costas, J., Vakharia, V. N., and Benavente, J. (2004). Avian reovirus nonstructural protein microNS forms viroplasm-like inclusions and recruits protein sigmaNS to these structures. Virology 319, 94-106. doi: 10.1016/j.virol.2003.10.034
83. Uyeda, I., Suda, N., Yamada, H., Kudo, H., Suga, H., Kimura, I., et al. (1994). Nucleotide sequence of rice dwarf phytoreovirus genome segment 2: completion of sequence analyses of rice dwarf virus. Intervirology 37, 6-11. doi:10.1159/000150348
84. Vazquez Rovere, C., del Vas, M., and Hopp, H. E. (2002). RNA mediated virus resistance. Curr. Opin. Biotechnol. 13, 167-172. doi: 10.1016/S0958-1669(02)00296-3
85. Voinnet, O. (2005). Induction and suppression of RNA silencing: insights from viral infections. Nat. Rev. Genet. 6, 206-220. doi: 10.1038/nrg1555
86. Voinnet, O., Lederer, C., and Baulcombe, D. C. (2000). A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103, 157-167. doi: 10.1016/S0092-8674(00)00095-7
87. Wang, H. D., Zhu, J. L., and Zhu, L. M. (2007). Efficient application of pesticides to control the small brown planthopper, Laodelphax striatellus, on rice. Chin. Rice Gra. 3, 59-60.
88. Wang, M. B., Abbott, D. C., and Waterhouse, P. M. (2000). A single copy of a virus-derived transgene encoding hairpin RNA gives immunity to Barley yellow dwarf virus. Mol. Plant Pathol. 1, 347-356. doi: 10.1046/j.1364-3703.2000.00038.x
89. Wang, Z. C., Yu, D. D., Li, X. Y., Zeng, M. J., Chen, Z., Bi, L., et al. (2012). The development and application of a dot-ELISA assay for diagnosis of southern rice black-streaked dwarf disease in the field. Viruses 4, 167-183. doi: 10.3390/v4010167
90. Wei, T., Shimizu, T., Hagiwara, K., Kikuchi, A., Moriyasu, Y., Suzuki, N., et al. (2006). Pns12 protein of Rice dwarf virus is essential for formation of viroplasms and nucleation of viral-assembly complexes. J. Gen. Virol. 87, 429-438. doi: 10.1099/vir.0.81425-0
91. Wu, Z., Wu, J., Adkins, S., Xie, L., and Li, W. (2010). Rice ragged stunt virus segment 6-encoded nonstructural protein Pns6 complements cell-to-cell movement of tobacco mosaic virus-based chimeric virus. Virus Res. 152, 176-179. doi: 10.1016/j.virusres.2010.06.003
92. Xiong, R., Wu, J., Zhou, Y., and Zhou, X. (2009). Characterization and subcellular localization of an RNA silencing suppressor encoded by Rice stripe Tenuivirus. Virology 387, 29-40. doi: 10.1016/j.virol.2009.01.045
93. Xiong, R., Wu, J., Zhou, Y., and Zhou, X. (2008). Identification of a movement protein of the Tenuivirus Rice stripe virus. J. Virol. 82, 12304-12311. doi: 10.1128/JVI.01696-08
94. Zhang, L., Wang, Z., Wang, X., Li, D., Han, C., Zhai, Y., et al. (2005). Two virus-encoded RNA silencing suppressors, P14 of Beet necrotic yellow vein virus and S6 of Rice black streak dwarf virus. Chin. Sci. Bull. 50, 305-310.
95. Zhang, Y. X., Wang, Q., Jiang, L., Liu, L. L., Wang, B. X., Shen, Y. Y., et al. (2011). Fine mapping of qSTV11(KAS), a major QTL for rice stripe disease resistance. Theor. Appl. Genet. 122, 1591-1604. doi: 10.1007/s00122-011-1557-0
96. Zeigler, R., and Barclay, A. (2008). The relevance of rice. Rice 1, 3-10. doi: 10.1007/s12284-008-9001-z
97. Zhong, B., Kikuchi, A., Moriyasu, Y., Higashi, T., Hagiwara, K., and Omura, T. (2003). A minor outer capsid protein, P9, of Rice dwarf virus. Arch. Virol. 148, 2275-2280. doi: 10.1007/s00705-003-0160-3
98. Zhu, Y., Hayakawa, T., Toriyama, S., and Takahashi, M. (1991). Complete nucleotide sequence of RNA 3 of rice stripe virus: an ambisense coding strategy. J. Gen. Virol. 72, 763-767. doi: 10.1099/0022-1317-72-4-763