Biotechnological approaches for plant viruses resistance: From general to the modern RNA silencing pathway

Brazilian Archives of Biology and Technology

Volumn 52, Issue 4, 2009, Pages 795-808

  Rodrigues, Silas Pessini ^a   Lindsey, George G ^b   Bueno Fernandes, Patricia Machado ^a  

^a FEDERAL UNIVERSITY OF ESPÍRITO SANTO   (Brazil)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Engineered resistance; Phytopathogens; Plant defense

Indexed keywords

EID: 77649165381     PISSN: 15168913     EISSN: 15168913     Source Type: Journal    
DOI: 10.1590/S1516-89132009000400002     Document Type: Review

References (135)

1. Ascencio-Ibáñez, J.T.; Sozzani, R.; Lee, T.J.; Chu, T.M.; Wolfinger, R.D.; Cella, R.; Hanley-Bowdoin, L. (2008), Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol., 148, 436-454.
2. Andika, I.B.; Kondo, H.; Tamada, T. (2005), Evidence that RNA silencing-mediated resistance to Beet necrotic yellow vein virus is less effective in roots than in leaves. Mol. Plant Microbe Interact., 18, 194-204.
3. Asurmendi, S.; Bergi, R.H.; Koo, J.C.; Beachy, R.N. (2004), Coat protein regulates formation of replication complex during tobacco mosaic virus infection. Proc. Natl. Acad. Sci. USA, 101, 1415-1420.
4. Audy, P.; Palukaitis, P.; Slack, S.A.; Zaitlin, M. (1994), Replicase-mediated resistance to Potato virus Y in transgenic plants. Mol. Plant Microbe Interact., 7, 18-22.
5. Azevedo, C.; Sadanandom, A.; Kitagawa, K.; Freialdenhoven, A.; Shirasu, K.; Schulze-Lefert, P. (2002), The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science, 295, 2073-2076.
6. Balachandran. S.; Hurry. V.M.; Kelley, S.E.; Osmond, C.B.; Robinson, S.A.; Rohozinski, J.; Seaton, G.G.R.; Sims, D.A. (1997), Concepts of plant biotic stress. Some insights into the stress physiology of virus-infected plants, from the perspective of photosynthesis. Physiologia Plantarum, 100, 203-213.
7. Baker, B.; Zambryski, P.; Staskawicz, B.; Dinesh-Kumar, S.P. (1997), Signaling in plant-microbe interaction. Science, 276, 726-733.
8. Bartel, D.P. (2004), MicroRNAs: genomics, biogenesis, mechanisms, and functions. Cell, 116, 281-297.
9. Baulcombe, D. (1996), Mechanisms of pathogen-derived resistance to viruses in transgenic plants. Plant Cell, 8, 1833-1844.
10. Beachy, R.N. (1994), Introduction: transgenic resistance to plant viruses. Semin. Virol., 4, 327-328.
11. Beachy, R.N. (1997), Mechanisms and applications of pathogen-derived resistance in transgenic plants. Curr. Opin. Biotechnol., 8, 215-220.
12. Belkhadir, Y.; Subramaniam, R.; Dangl, J.L. (2004); Plant disease resistance protein signaling: NBS-LRR proteins and theirs partners. Curr. Opin. Plant Biol., 7, 391-399.
13. Bendahmane, M.; Szécsi, J.; Chen, I.; Berg, R.H.; Beachy, R.N. (2002), Characterization of mutant tobacco mosaic virus coat protein that interferes with virus cell-to-cell movement. Proc. Natl. Acad. Sci. USA, 99, 3645-3650.
14. Bertacini, P.V.; Álvaro, M.R.; Almeida, J.; Albérsio, A.L.; Chagas, C.M. (1998), Biological and Physicochemical Properties of Cowpea Severe Mosaic Comovirus Isolated from Soybean in the State of Paraná. Brazilian Archives of Biology and Technology, 4, 409-416.
15. Brederode, F.T.; Tsachner, P.E.M.; Posthumus, E.; Bol, J.F. (1995), Replicase-mediated resistance to alfafa mosaic virus. Virology, 207, 467-474.
16. Borém, A.; Milach, S.C.K. (1998), Plant Breeding in the Turn of the Millenium. Brazilian Archives of Biology and Technology, 3, 278-283.
17. Brodersen, P.; Voinnet, O. (2006), The diversity of RNAsilencing pathways in plants. Trends Genet., 22, 268-280.
18. Cao, X. ; Aufsatz, W.; Zilberman, D.; Mette, M.F.; Huang, M.S.; Matzke, M.; Jacobsen, S.E. (2003), Role of the RDM and CTM3 methyltranferases in RNA-directed DNA methylation. Curr. Biol., 13, 2212-2217.
19. Cao, X.; Springer, N.M.; Muszynski, M.G.; Phillips, R.L.; Kaeppler, S.; Jacobsen, S.E. (2000), Conserved plant genes with similarity to mammalian de novo DNA methyltransferases. Proc. Natl. Acad. Sci. USA, 97, 4979-4984.
20. Cannell, I.G.; Kong, Y.W.; Bushell, M. (2008), How do microRNAs regulate gene expression? Biochem Soc Trans., 36, 1224-1231.
21. Carmell, M.A.; Hannon, G.J. (2004), RNase III enzyme and the initiator of gene silencing. Nat. Struct. Mol. Biol., 11, 214-218.
22. Carmell, M.A.; Xuan, Z.; Zhang, M.Q.; Hannon, G.J.; (2002), The Argonaute family: tentacles that reach into RNAi, development control, stem-cell maintenance, and tumorigenesis. Genes Dev., 16, 2733-2743.
23. Castle, S.; Palumbo, J.; Prabhaker, N. (2009), Newer insecticides for plant virus disease management. Virus Res., doi:10.1016/j.virusres.2008.12.006.
24. Cavatorta, J.R.; Savage, A.E.; Yeam, I.; Gray, S.M.; Jahn, M.M. (2008), Positive Darwinian selection at single amino acid sites conferring plant virus resistance. J Mol Evol., 67, 551-559.
25. Cerqueira-Silva, C.B.; Moreira, C.N.; Figueira, A.R.; Corrêa, R.X.; Oliveira, A.C. (2008), Detection of a resistance gradient to Passion fruit woodiness virus and selection of 'yellow' passion fruit plants under field conditions. Genet Mol Res., 7, 1209-1216.
26. Cooper, D.; Lapidot, M.; Heick, H.A.; Dodde, J.A.; Beachy, R.N. (1995), Multi-virus resistance in transgenic tobacco plants expressing a dysfunctional movement protein of tobacco mosaic. Virology, 206, 307-313.
27. Crawford, K.M.; Zambryski, P.C. (1999), Plasmodesmata signaling: many roles, sophisticated statutes. Curr. Opn. Plant Biol., 2, 382-387.
28. Diaz-Pendon, J.A.; Truniger, V.; Nieto, C.; Gracia-Mas, J.; Bendahmane, A.; Aranda, M.A. (2004), Advances in understanding recessive resistance to viruses. Mol. Plant Pathol., 5, 223-233.
29. Dangl, J.L.; McDowell, J.M. (2006), Two modes of pathogen recognition by plants. Proc. Natl. Acad. Sci. U S A., 103, 8575-8576.
30. Dieryck, B.; Otto, G.; Doucet, D.; Legrève, A.; Delfosse, P.; Bragard, C. (2009), Seed, soil and vegetative transmission contribute to the spread of pecluviruses in Western Africa and the Indian sub-continent. Virus Res., doi:10.1016/j.virusres.2008.08.017.
31. Dong, Z.; Han, M.H.; Fedoroff, N. (2008), The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proc Natl Acad Sci U S A., 105, 9851-9852.
32. Drake, J.W.; Holland, J.J. (1999), Mutation rates among RNA viruses. Proc. Natl. Acad. Sci. USA, 96, 13910-13913.
33. Duan, C.G.; Wang, C.H.; Fang, R.X.; Guo, H.S. (2008), Artificial MicroRNAs highly accessible to targets confer efficient virus resistance in plants. J Virol., 82, 11084-11095.
34. Elbashir, S.M.; Lendeckel, W.; Tuschi, T. (2001), RNA interference is mediated by 21 and 22 nt RNAs. Genes Dev., 15, 188-200.
35. Elgin, S.C.R.; Grewal, S.I.S. (2003), Heterochromatin: silence is golden. Curr. Biol., 13, 895-898.
36. Ellis, J.G.; Dodds, P.N.; Lawrence, G.J. (2007), Flax rust resistance gene specificity is based on direct resistance-avirulence protein interactions. Annu Rev Phytopathol., 45, 289-306.
37. Fereres, A.; Moreno, A. (2009), Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Res., doi:10.1016/j.virusres.2008.10.020.
38. Finlay, K.W. (1953), Inheritance of spotted wild resistance in the tomato II. Five genes controlling spotted wild resistance in four tomato types. Aust. J. Biol. Sci., 6, 153.
39. Finnegan, E.J.; Margis, R.; Waterhouse, P.M. (2003), Posttranscriptional gene silencing is not compromised in the Arabidopsis CARPEL FACTORY (DICER-LIKE 1) mutant, a homolog of Dicer-1 from Drosophila. Curr. Biol., 13, 236-240.
40. Fraser, R.S.S. (1992), The genetics of plant virus interactions: implication for plant breeding. Euphytica, 63, 175-185.
41. Freitag, M.; Lee, D.W.; Kothe, G.O.; Pratt, R.J.; Aramayo, R.; Selker, E.U. (2004), DNA methylation is dependent of RNA interference in Neurospora. Science, 304, 1939.
42. Gao, Z.; Johansen, E.; Eyers, R.; Thomas, C.L.; Noel Ellis, T.H.; Maule, A.J. (2004), The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J., 40, 376-385.
43. Garcia, D. (2008), A miRacle in plant development: role of microRNAs in cell differentiation and patterning. Semin Cell Dev Biol., 19, 586-595.
44. Gharsallah Chouchane, S.; Gorsane, F.; Nakhla, M.K.; Salus, M.; Martin, C.T.; Maxwell, D.P.; Marrakchi, M.; Fakhfakh, H. (2008), Evaluation of two gene-silencing constructs for resistance to tomato yellow leaf curl viruses in Nicotiana benthamiana plants. Acta Virol., 52, 143-149.
45. Gilligan, C.A.; van den Bosch, F. (2008), Epidemiological models for invasion and persistence of pathogens. Annu Rev Phytopathol., 46, 385-418.
46. Gutierrez, C. (2000), DNA replication and cell cycle in plants: learning from geminiviruses. EMBO J., 19, 792-799.
47. Hagiwara, Y.; Komoda, K.; Yamanaka, T.; Tamai. A.; Meshi, T.; Funada, R.; Tsuchiya, T.; Naito, S.; Ishikawa, M. (2003), Subcellular localization of host and viral proteins associated with tobamovirus RNA replication. EMBO J., 22, 344-353.
48. Hamilton, A.; Voinnet, O.; Chappell, L.; Baulcombe, D. (2002), Two classes of short interfering RNA in RNA silencing. EMBO J., 21, 4671-4679.
49. Hammond, S.M.; Bernstein, E.; Beach, D.; Hannon, G.J. (2000), An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosiphila cells. Nature, 404, 293-296.
50. Hammond-Kosack, K.E.; Jones, J.D. (1997), Plant resistance genes. Annu. Rev. Plant Physiol. Plant Mol. Biol., 48, 575-607.
51. Han, M.H.; Goud, S.; Song, L.; Fedoroff, N. (2004), The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc. Natl. Acad. Sci. USA, 101, 1093-1098.
52. He, X.J.; Hsu, Y.F.; Pontes, O.; Zhu, J.; Lu, J.; Bressan, R.A.; Pikaard, C.; Wang, C.S.; Zhu, J.K. (2009), NRPD4, a protein related to the RPB4 subunit of RNA polymerase II, is a component of RNA polymerases IV and V and is required for RNA-directed DNA methylation. Genes Dev., 23, 318-330.
53. Hills, G.H.; Plaskitt, K.A.; Young, N.D.; Dunigan, D.D.; Watts, J.W.; Wilson, T.M.A.; Zaitlin, M. (1987), Immunogold localization of the intracellular sites of structural and nonstructural tobacco mosaic virus proteins. Virology, 161, 488-496.
54. Hubert, D.A.; Tornero, P.; Belkhadir, Y.; Krishna, P.; Takahashi, A.; Shirasu, K.; Dangl, J.L. (2003), Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J., 22, 5679-5689.
55. Ichiki, T.U.; Nagaoka, E.N.; Hagiwara, K.; Uchikawa, K.; Tsuda, S.; Omura, T. (2005), Integration of mutations responsible for the attenuated phenotype of Pepper mild mottle virus strains results in a symptomless cross-protecting strain. Arch Virol., 150, 2009-2020.
56. Iriti, M.; Faoro, F. (2007), Review of innate and specific immunity in plants and animals. Mycopathologia, 164, 57-64.
57. Jackson, J.P.; Lindroth, A.M.; Cao, X.; Jacobsen, S.E. (2002), Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature, 416, 556-560.
58. Jia, Y.; McAdams, S.A.; Bryan, G.T.; Hershey, H.P.; Valent, B. (2000), Direct interaction of resistance gene and avirulence gene products confers rise blast resistance. EMBO J., 19, 4004-4014.
59. Johansen, L.K.; Carrington, J.C. (2001), Silencing on the spot. Induction and suppression of RNA silencing in Agrobacterium-mediated transient expression system. Plant Physiol., 126, 930-938.
60. Jones, A.L.; Thomas. C.L.; Maule, A.J. (1998), De novo methylation and co-suppression induced by a cytoplasmically replicating plant RNA virus. EMBO J., 17, 6385-6393.
61. Jones, R.A. (2009), Plant virus emergence and evolution: Origins, new encounter scenarios, factors driving emergence, effects of changing world conditions, and prospects for control. Virus Res., doi:10.1016/j.virusres.2008.07.028.
62. Kang, B.C.; Yeam, I.; Frantz, J.D.; Murphy, J.F.; Jahn, M.M. (2005a), The pvr1 locus in pepper encodes a translation initiation factor eIF4E that interact with Tobacco etch virus VPg. Plant J., 42, 392-405.
63. Kang, B.C.; Yeam, I.; Jahn, M.M. (2005), Genetics of plant virus resistance. Annu. Rev. Phytopathol., 43, 581-621.
64. Kawasaki, H.; Taira, K. (2004), Induction of DNA methylation and gene silencing by short interfering RNAs in human cells. Nature, 431, 211-217.
65. Keller, K.E.; Johansen, I.E.; Hampton, R.O.; Martin, R.R. (1996), A recessive plant resistance gene governs the action of a putative potyvirus replication genome. Phytopathology, 86, S18.
66. Keese, P. (2008), Risks from GMOs due to horizontal gene transfer. Environ Biosafety Res., 7, 123-149.
67. Kehr, J.; Buhtz, A. (2008), Long distance transport and movement of RNA through the phloem. J Exp Bot., 59, 85-92.
68. Kobayashi, K.; Otegui, M.S.; Krishnakumar, S.; Mindrinos, M.; Zambryski, P. (2007), INCREASED SIZE EXCLUSION LIMIT 2 encodes a putative DEVH box RNA helicase involved in plasmodesmata function during Arabidopsis embryogenesis. Plant Cell., 19, 1885-1897.
69. Lecoq, H.; Moury, B.; Desbiez, C.; Palloix, A.; Pitrat, M. (2004), Durable viral resistance in plants through conventional approaches: a challenge. Virus Research, 100, 31-39.
70. Lee, W.M.; Ishikawa, M.; Ahlquist, P. (2001), Mutation of host Δ9 fatty acid desaturase inhibits brome mosaic virus RNA replication between template recognition and RNA synthesis. J. Virol., 75, 2097-2106.
71. Leonard, S.; Plante, D.; Wittmann, S.; Daigneault, N.; Fortin, M.G.; Laliberte, J.F. (2000), Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. J. Virol., 74, 7730-7737.
72. Lippman, Z.; May, B.; Yordan, C.; Singer, T.; Martienssen, R. (2003), Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol., 1, E67.
73. Liu, J.; Carmell, M.A.; Rivas, F.V.; Marsden, C.G.; Thomson, J.M.; Song, J.; Hammond, S.M.; Joshua-Tor, L.; Hannon, G.J. (2004), Argonaute2 is the catalytic engine of mammalian RNAi. Science, 303, 1437-1441.
74. Lough, T.J.; Lucas, W.J. (2006), Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu. Rev. Plant Biol., 57, 203-32.
75. Lózsa, R.; Csorba, T.; Lakatos, L.; Burgyán, J. (1999), Inhibition of 3' modification of small RNAs in virus-infected plants require spatial and temporal co-expression of small RNAs and viral silencing-suppressor proteins. Nucleic Acids Res., 36, 4099-4107.
76. Lu, R.; Malcuit, I.; Moffett, P.; Ruiz, M.T.; Peart, J.; Wu, A.J.; Rathjen, J.P.; Bendahmane, A.; Day, L.; Baulcombe, D.C. (2003), High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J., 22, 5690-5699.
77. Lucas, W.J. (2006), Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology, 344, 169-184.
78. Lund, E.; Guttinger, S.; Calado, A.; Dahlberg, J.E.; Kutay, U. (2004), Nuclear export of microRNA precursor. Science, 303, 95-98.
79. Ma, G.; Chen, P. ; Buss, G.R. ; Tolin, S.A. (2004), Genetics of resistance to two strains of soybean mosaic virus in differential soybean genotypes. J Hered., 95, 322-326.
80. Mangrauthia, S.K.; Parameswari, B.; Jain, R.K.; Praveen, S. (2008), Role of genetic recombination in the molecular architecture of Papaya ringspot virus. Biochem Genet., 46, 835-846.
81. Malnoe, P.; Farinelli, L.; Collet, G.F.; Reust, W. (1994), Small-scale field test with transgenic potato, cv. Bintje, to test resistance to primary and second infections with Potato virus Y. Plant Mol. Biol., 25, 963-975.
82. Martin, G.B.; Bogdanove, A.J.; Sessa, G. (2003), Understanding the functions of plant resistance proteins. Annu. Rev. Plant Biol., 54, 23-61.
83. Masuta, C.; Kuwata, S.; Matzuzaki, T.; Takanami, Y.; Koiwai, A. (1992), A plant virus satellite RNA exhibits a significant sequence complementary to a chloroplast tRNA. Nucleic Acids Res., 20, 2885.
84. Mathieu, O.; Bender, J. (1991), RNA-directed DNA methylation. J. Cell Science, 117, 4881-4888.
85. Mayo, M.A.; Jolly, C.A. (1991), The 5′-terminal sequence of Potato leafroll virus RNA: evidence of recombination between virus and host RNA. J. Gen Virol., 72, 2591-2595.
86. MCLean, B.G.; Hempel, F.D.; Zambryski, P.C. (1997), Plant intercellular communication via plasmodesmata. Plant Cell, 9, 1043-1054.
87. Michael, T.; Wilson, A. (1993) Strategies to protect crop plants against viruses: Pathogen-derived resistance blossoms. Proc. Natl. Acad. Sci. USA, 99, 3134-3141.
88. Miller, W.A.; Koev, G.; Mohan, B.R. (1997), Are there risks associated to resistance to luteoviruses? Plant Dis., 81, 700-710.
89. Miller, E.D.; Hemenway, C. (1998), History of coat protein-mediated protection. Methods Mol Biol., 81, 25-38.
90. Morroni, M.; Thompson, J.R.; Tepfer, M. (2008), Twenty years of transgenic plants resistant to Cucumber mosaic virus. Mol Plant Microbe Interact., 21, 675-684.
91. Mlotshwa, S.; Pruss, G.J.; Vance, V. (2008), Small RNAs in viral infection and host defense. Trends Plant Sci., 13, 375-382.
92. Napoli, C.; Lemieux, C.; Jorgensen, R. (1990), Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell, 2, 279-289.
93. Naqvi, A.R.; Islam, M.N.; Choudhury, N.R.; Haq, Q.M. (2009), The fascinating world of RNA interference. Int J Biol Sci., 5, 97-117.
94. Nicaise, V.; German-Retana, S.; Sanjuán, R.; Dubrana, M.P.; Mazier, M.; Maisonneuve, B.; Candresse, T.; Caranta, C.; LeGall, O. (2003), The eukaryotic translation initiator factor 4E controls lettuce susceptibility to the potyvirus lettuce mosaic virus. Plant Physiol., 132, 1272-1282.
95. Novy, R.G.; Gillen, A.M.; Whitworth, J.L. (2008), Characterization of the expression and inheritance of potato leafroll virus (PLRV) and potato virus Y (PVY) resistance in three generations of germplasm derived from Solanum etuberosum. Theor Appl Genet., 114, 1161-1172.
96. Papp, I.; Mette, M.F.; Austsatz, W.; Daxinger, L.; Schauer, S.E.; Ray, A.; van der Winder, J.; Matzke, M.; Matzke, A.J.M. (2003), Evidence for nuclear processing of plant micro RNA and short interfering RNA precursors. Plant Physiol., 132, 1382-1390.
97. Pantaleo, V.; Szittya, G.; Burgyán, J. (1999), Molecular bases of viral RNA targeting by viral small interfering RNA-programmed RISC. J Virol., 81, 3797-3806.
98. Pélissier, T.; Thalmeir, S.; Kempe, D.; Sänger, H.L.; Wassenegger, M. (1999), Heavy de novo methylation at symmetrical and non-symmetrical sites is a hallmark of RNA-directed DNA methylation. Nucleic Acids Res., 27, 1625-1634.
99. Powell, A.P.; Nelson, R.S.; De, B.; Holfmann, N.; Rogers, S.G.; Fraley, R.T.; Beachy, R.N. (1986), Delay of disease development in transgenic plants that express the Tobacco mosaic virus coat protein gene. Science, 232, 738-743.
100. Pruss, G.J.; Lawrence, C.B.; Bass, T.; Li, Q.Q.; Bowman, L.H.; Vance, V. (2004), The potyviral suppressor of RNA silencing confers resistance to multiple pathogens. Virology, 320, 107-120.
101. Prins, M.; Laimer, M.; Noris, E.; Schubert, J.; Wassenegger, M.; Tepfer, M. (2008), Strategies for antiviral resistance in transgenic plants. Mol Plant Pathol., 9, 73-83.
102. Qu, F.; Ye, X.; Morris, T.J. (2008), Arabidopsis DRB4, AGO1, AGO7, and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. Proc Natl Acad Sci U S A., 105, 14732-14737.
103. Ritzenthaler, C. (2005), Resistance to plant viruses: old issues, news answers? Current Oppin. Plant Biothecnology, 16, 118-122.
104. Rivas, F.V.; Tolia, N.H.; Song, J.J.; Aragon, J.P.; Liu, J.; Hannon, G.J.; Joshua-Tor, L. (2005), Purified Argonaute2 and siRNA form recombinant human RISC. Nat. Struct. Mol. Biol., 12, 340-349.
105. Rodrigues, S.P.; Andrade, J.S.; Ventura, J.A.; Lindsey, G.G.; Fernandes, P.M.B. (2009a), Papaya meleira virus is neither transmitted by infection at wound sites nor by the whitefly Trialeurodes variabilis. J Plant Pathol., 91, 87-91.
106. Rodrigues, S.P.; Ventura, J.A.; Da Cunha, M., Fernandes, P.M.B. (2009b), Effects of Papaya meleira virus on papaya latex structure and composition. Plant Cell Rep., DOI 10.1007/s00299-009-0673-7.
107. Ruiz-Ferrer, V.; Voinnet, O. (2008), Roles of Plant Small RNAs in Biotic Stress Responses. Annu Rev Plant Biol., doi:10.1146/annurev.arplant.043008.092111.
108. Saze, H.; Scheid, O.M.; Paszkowski, J. (2003), Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat. Genet., 34, 65-69.
109. Shirasu, K.; Lahaye, T.; Tan, M.W.; Zhou, F.; Azevedo, C.; Schulze-Lefert, P. (1999), A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell, 99, 355-366.
110. Shibuya, K.; Fukushima, S.; Takatsuji, H. (2009), RNA-directed DNA methylation induces transcriptional activation in plants. Proc Natl Acad Sci U S A., 106, 1660-1665.
111. Takahashi, A.; Casais, C.; Ichimura, K.; Shirasu, K. (2003), HSP90 interacts with RAR1 and SGT1 and is essential fro RPS2-mediated disease resistance in Arabidopsis. Proc. Natl. Acad. Sci. USA, 100, 11777-11782.
112. Taliansky, M.; Torrance, L.; Kalinina, N.O. (2008), Role of plant virus movement proteins. Methods Mol Biol., 451, 33-54.
113. Tang, G.; Reinhart, B.J.; Bartel, D.P.; Zamore, P.D. (2003), A biochemical framework for RNA silencing in plants. Genes Dev., 17, 49-63.
114. Tepfer, M. (2002), Risk assessment of virus-resistant transgenic plants. Annu. Rev. Phytopathol., 40, 467-491.
115. Tenllado, F.; Martínez-Gracia, B.; Vargas, M.; Díaz-Ruíz, J.R. (2003), Crude extracts of bacterially expressed dsRNA can be used to protect plants against virus infections. BMC Biotechnol., 3, 1-11.
116. Tenllado, F.; Llave, C.; Díaz-Ruíz, J.R. (2004), RNA interference as a new biotechnological tool for the control of virus diseases in plants. Virus Res., 102, 85-96.
117. Tennant, P.F.; Gonsaives, C.; Ling, K.S.; Fitch, M.; Manshardt, R.; Slightom, J.L.; Gonsalves, D. (1994), Differential protection against papaya ringspot virus isolates in coat protein gene transgenic papaya and classically cross-protected papaya. Phytopathology, 84, 1359-1366.
118. Timmons, L.; Fire, A. (1998), Specific interference by ingested dsRNA. Nature, 395, 854.
119. Tsujimoto, Y.; Numaga, T.; Ohshima, K.; Yano, M,A.; Ohsawa, R.; Goto, D.B.; Naito, S.; Ishikawa, M. (2003), Arabidopsis TOBAMOVIRUS MULTIPLICATION (TOM) 2 locus encodes a transmembrane protein that interact with TOM1. EMBO J., 22, 335-343.
120. Vaistji, F.E. ; Jones, L.; Baulcombe, D.C. (2002), Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA-dependent RNA polymerase. Plant Cell, 14, 857-867.
121. Varrelmann, M.; Maiss, E. (2000), Mutation in the coat protein gene of Plum pox virus suppress particle assembly, heterologous encapsidation and complementation in transgenic plants of Nicotiana benthamiana. J. Gen. Virol., 81, 567-577.
122. Vaucheret, H.; Vazquez, F.; Crete, P.; Bartel, D.P. (2004), The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev., 18, 1187-1197.
123. Vaucheret, H. (1999), Plant ARGONAUTES. Trends Plant Sci., 13, 350-358.
124. Ventura, J.A.; Costa, H.; Tatagiba, J. (2004), Papaya diseases and integrated control. In: Naqvi, S.A.H. (ed) Diseases of fruits and vegetables: diagnosis and management. Kluwer, London
125. Voinnet, O. (2001), RNA silencing as a plant immune system against viruses. Trends Genet., 17, 449-459.
126. Wang, D.; Maule, A.L. (1995), Inhibition of host genes expression associated with plant virus replication. Science, 267, 229-231.
127. Wang, M.B.; Metzlaff, M. (2005), RNA silencing and antiviral defense in plants. Curr. Opin. Plant Biol., 8, 216-222.
128. Wang, M.B.; Wesley, S.V.; Finnegan, E.J.; Smith, N.A.; Waterhouse, P.M. (2001), Replicating satellite RNA induces sequence-specific DNA methylation and truncated transcripts in plants. RNA, 7, 16-28.
129. Waterhouse, P.M.; Wang, M.B.; Lough, T. (2001), Gene silencing as an adaptive defense against viruses. Nature, 411, 834-842.
130. Xie, Z.; Allen, E.; Wilken, A.; Carrington, J.C. (2005), DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA, 102, 12984-12989.
131. Xie, Z.; Johansen, L.K.; Gustafson, A.M.; Kasschau, D.; Lellis, A.D.; Zilberman, D.; Jacobsen, S.E.; Carrington, J.C. (2004), Genetic and functional diversification of small RNA pathways in plants. PLoS. Biol., 2, E104.
132. Xie, Z,; Qi, X. (2008), Diverse small RNA-directed silencing pathways in plants. Biochim Biophys Acta., 1779, 720-724.
133. Yamanaka, T.; Ohta, T.; Takahashi, M.; Meshi, T.; Schmidt, R.; Dean, C.; Naito, S.; Ishikawa, M. (2000), TOM1, an Arabdopsis gene required fro transmembrane protein. Proc. Natl. Acad. Sci. USA, 97, 10107-10112.
134. Yoshikawa, N.; Saitou, Y.; Kitajima, A.; Chida, T.; Sasaki, N.; Isogai, M. (2006), Interference of Long-Distance Movement of Grapevine berry inner necrosis virus in Transgenic Plants Expressing a Defective Movement Protein of Apple chlorotic leaf spot virus. Phytopathology, 96, 378-385.
135. Zaitlin, M.; Anderson, J.M.; Parry, K.L.; Zhang, L.; Palukaitin, P. (1994), Specificity of replicase-mediated resistance to cucumber mosaic virus. Virology, 201, 200-205.