The pathogenicity determinant of Citrus tristeza virus causing the seedling yellows syndrome maps at the 3′-terminal region of the viral genome

Molecular Plant Pathology

Volumn 11, Issue 1, 2010, Pages 55-67

  Albiach Marti, Maria R ^a   Robertson, Cecile ^b   Gowda, Siddarame ^b   Tatineni, Satyanarayana ^b   Belliure, Belén ^a   Garnsey, Stephen M ^b   Folimonova, Svetlana Y ^b   Moreno, Pedro ^a   Dawson, William O ^b  

^a INSTITUTO VALENCIANO DE INVESTIGACIONES AGRARIAS IVIA   (Spain)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CITRUS FRUIT; GENETICS; PATHOGENICITY; PLANT DISEASE; PLANT VIRUS; VIROLOGY; VIRUS GENOME;

CITRUS; GENOME, VIRAL; PLANT DISEASES; PLANT VIRUSES;

CITRUS; CITRUS AURANTIUM; CITRUS LIMON; CITRUS MACROPHYLLA; CITRUS TRISTEZA VIRUS; CITRUS X PARADISI; CLOSTEROVIRIDAE; CLOSTEROVIRUS; NICOTIANA BENTHAMIANA;

EID: 73649105508     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2009.00572.x     Document Type: Article

References (53)

1. Albiach-Martí, M.R., Guerri, J., Cambra, M., Garnsey, S.M. Moreno, P. (2000a) Differentiation of citrus tristeza virus isolates by serological analysis of the p25 coat protein peptide maps. J. Virol. Methods, 88, 25 34.
2. Albiach-Martí, M.R., Guerri, J., Hermoso de Mendoza, A., Laigret, F., Ballester-Olmos, J.F. Moreno, P. (2000b) Aphid transmission alters the genomic and defective RNA populations of citrus tristeza virus. Phytopathology, 90, 134 138.
3. Albiach-Martí, M.R., Mawassi, M., Gowda, S., Satyanarayana, T., Hilf, M.E., Shanker, S., Almira, E.C., Vives, M.C., López, C., Guerri, J., Flores, R., Moreno, P., Garnsey, S.M. Dawson, W.O. (2000c) Sequences of Citrus tristeza virus separated in time and space are essentially identical. J. Virol. 74, 6856 6865.
4. Bar-Joseph, M. Dawson, W.O. (2008) Citrus tristeza virus. In : Encyclopedia of Virology, Vol. 1 (Mahy, B.W.J. Van Regenmortel, M.H.V., eds), pp. 520 525. Oxford : Elsevier Ltd.
5. Bar-Joseph, M., Marcus, R. Lee, R.F. (1989) The continuous challenge of citrus tristeza virus control. Annu. Rev. Phytopathol. 27, 291 316.
6. Batuman, O., Mawassi, M. Bar-Joseph, M. (2006) Transgenes consisting of a dsRNA of an RNAi suppressor plus the 3′UTR provide resistance to Citrus tristeza virus sequences in Nicotiana benthamiana but not in citrus. Virus Genes, 33, 319 327.
7. Broadbent, P., Bevington, K.B. Coote, B.G. (1991) Control of stem pitting of grapefruit in Australia by mild strain cross protection. In : Proceedings of the 11th Conference of the International Organization of Citrus Virologists (Brlansky, R.H., Lee, R.F. Timmer, L.W., eds), pp. 64 70. Riverside, CA : International Organization of Citrus Virologists.
8. Chapman, E.J., Prokhnevsky, A.I., Gopinath, K., Dolja, V.V. Carrington, J.C. (2004) Viral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step. Genes Dev. 18, 1179 1186.
9. Costa, A.S. Müller, G.W. (1980) Tristeza control by cross protection: a US-Brazil cooperative success. Plant Dis. 64, 538 541.
10. Dolja, V.V., Kreuze, J.F. Valkonen, J.P. (2006) Comparative and functional genomics of closteroviruses. Virus Res. 117, 38 51.
11. Dunoyer, P., Lecellier, C.-H., Parizotto, E.A., Himber, C. Voinnet, O. (2004) Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell, 16, 1235 1250.
12. Fagoaga, C., López, C., Moreno, P., Navarro, L., Flores, R. Peña, L. (2005) Viral-like symptoms induced by the ectopic expression of the p23 of Citrus tristeza virus are citrus specific and do not correlate with the pathogenicity of the virus strain. Mol. Plant-Microbe Interact. 18, 435 445.
13. Fagoaga, C., López, C., Hermoso de Mendoza, A., Moreno, P., Navarro, L., Flores, R. Peña, L. (2006) Post-transcriptional gene silencing of the p23 silencing suppressor of Citrus tristeza virus confers resistance to the virus in transgenic Mexican lime. Plant Mol. Biol. 66, 153 165.
14. Folimonova, S.Y., Folimonov, A.S., Tatineni, S. Dawson, W.O. (2008) Citrus tristeza virus: survival at the edge of the movement continuum. J. Virol. 82, 6546 6556.
15. Fraser, L. (1952) Seedling yellows, an unreported virus disease of citrus. Agr. Gaz. N. S. W. 63, 125 131.
16. Fraser, R.S.S. (1998) Introduction to classical cross protection. In : Methods in Molecular Biology, Vol. 81, Plant Virus Protocols (Foster, D. Taylor, S.J. eds), pp. 13 24. Totowa, NJ : Humana Press.
17. Garnsey, S.M., Civerolo, E.L., Gumpf, D.J., Paul, C., Hilf, M.E., Lee, R.F., Brlansky, R.H., Yokomi, R.K. Hartung, J.S. (2005) Biological characterization of an international collection of Citrus tristeza virus (CTV) isolates. In : Proceedings of the 16th Conference of the International Organization of Citrus Virologists (Hilf, M.E., Duran-Vila, N. Rocha-Peña, M.A. eds), pp. 75 93. Riverside, CA : International Organization of Citrus Virologists.
18. Ghorbel, R., López, C., Moreno, P., Navarro, L., Flores, R. Peña, L. (2001) Transgenic citrus plants expressing the Citrus tristeza virus p23 protein exhibit viral-like symptoms. Mol. Plant Pathol. 2, 27 36.
19. Gowda, S., Satyanarayana, T., Davis, C.L., Navas-Castillo, J., Albiach-Martí, M.R., Mawassi, M., Valkov, N., Bar-Joseph, M., Moreno, P. Dawson, W.O. (2000) The p20 gene product of Citrus tristeza virus accumulates in the amorphous inclusion bodies. Virology, 274, 246 254.
20. Hilf, M.E., Karasev, A.V., Pappu, H.R., Gumpf, D.J., Niblett, C.L. Garnsey, S.M. (1995) Characterization of citrus tristeza virus subgenomic RNAs in infected tissue. Virology, 208, 576 582.
21. Hilf, M.E., Mavrodieva, V.A. Garnsey, S.M. (2005) Genetic marker analysis of a global collection of isolates of Citrus tristeza virus: characterization and distribution of CTV genotypes and association with symptoms. Phytopathology, 95, 909 917.
22. Karasev, A.V., Boyko, V.P., Gowda, S., Nikolaeva, O.V., Hilf, M.E., Koonin, E.V., Niblett, C.L., Cline, K., Gumpf, D.J., Lee, R.F., Garnsey, S.M., Lewandowski, D.J. Dawson, W.O. (1995) Complete sequence of the citrus tristeza virus RNA genome. Virology, 208, 511 520.
23. López, C., Ayllón, M.A., Navas-Castillo, J., Guerri, J., Moreno, P. Flores, R. (1998) Molecular variability of the 5′ and 3′ terminal regions of citrus tristeza virus RNA. Phytopathology, 88, 685 691.
24. López, C., Navas-Castillo, J., Gowda, S., Moreno, P. Flores, R. (2000) The 23-kDa protein coded by the 3′-terminal gene of citrus tristeza virus is an RNA-binding protein. Virology, 269, 462 470. (Pubitemid 30210918)
25. Lu, R., Folimonov, A., Shintaku, M., Li, W.X., Falk, B.W., Dawson, W.O. Ding, S.W. (2004) Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proc. Natl. Acad. Sci. USA, 101, 15 742 15 747.
26. Mawassi, M., Mietkiewska, E., Hilf, M.E., Ashoulin, L., Karasev, A.V., Gafny, A.V., Lee, R.F., Garnsey, S.M., Dawson, W.O. Bar-Joseph, M. (1995) Multiple species of defective RNAs in plants infected with citrus tristeza virus. Virology, 214, 264 268.
27. McClean, A.P.D. (1960) Seedling-yellows in South African citrus trees. S. Afr. J. Agric. Sci. 3, 259 279.
28. Moreno, P., Guerri, J. Muñoz, N. (1990) Identification of Spanish strains of citrus tristeza virus (CTV) by analysis of double-stranded RNAs (dsRNA). Phytopathology, 80, 477 482.
29. Moreno, P., Guerri, J., Ballester-Olmos, J.F., Albiach, R. Martínez, M.E. (1993) Separation and interference of strains from a citrus tristeza virus isolate evidenced by biological activity and double-stranded RNA (dsRNA) analysis. Plant Pathol. 42, 35 41.
30. Moreno, P., Ambrós, S., Albiach-Martí, M.R., Guerri, J. Peña, L. (2008) Plant diseases that changed the world - Citrus tristeza virus: a pathogen that changed the course of the citrus industry. Mol. Plant Pathol. 9, 251 268.
31. Navas-Castillo, J., Albiach-Martí, M.R., Gowda, S., Hilf, M.E., Garnsey, S.M. Dawson, W.O. (1997) Kinetics of accumulation of Citrus tristeza virus RNAs. Virology, 228, 92 97.
32. Pappu, H.R., Manjunath, K.L., Lee, R.F. Niblett, C.L. (1993) Molecular characterization of a structural epitope that is largely conserved among severe isolates of a plant virus. Proc. Natl. Acad. Sci. USA, 90, 3641 3644.
33. Qu, F. Morris, J. (2005) Suppressors of RNA silencing encoded by plant viruses and their role in viral infections. FEBS Lett. 579, 5958 5964.
34. Robertson, C.J., Garnsey, S.M., Satyanarayana, T., Folimonova, S. Dawson, W.O. (2005) Efficient infection of citrus plants with different cloned constructs of Citrus tristeza virus amplified in Nicotiana benthamiana protoplasts. In : Proceedings of the 16th Conference of the International Organization of Citrus Virologists (Hilf, M.E., Duran-Vila, N. Rocha-Peña, M.A. eds), pp. 187 195. Riverside, CA : International Organization of Citrus Virologists.
35. Rodríguez-Cerezo, E., Gamble Klein, P. Shaw, J.G. (1991) A determinant of disease symptom severity is located in the 3′-terminal noncoding regions of the RNA of a plant virus. Proc. Natl. Acad. Sci. USA, 88, 9863 9867.
36. Roistacher, C.N. Dodds, J.A. (1993) Failure of 100 mild Citrus tristeza virus isolates from California to cross protect against a challenge by severe sweet orange stem pitting isolates. In : Proceedings of the 12th Conference of the International Organization of Citrus Virologists (Moreno, P., da Graça, J. Timmer, L.W. eds), pp. 100 107. Riverside, CA : International Organization of Citrus Virologists.
37. Roistacher, C.N. Moreno, P. (1991) The worldwide threat from destructive isolates of citrus tristeza virus. A review. In : Proceedings of the 11th Conference of the International Organization of Citrus Virologists (Brlansky, R.H., Lee, R.F. Timmer, L.W. eds), pp. 7 19. Riverside, CA : International Organization of Citrus Virologists.
38. Sambade, A., López, C., Rubio, L., Flores, R., Guerri, J. Moreno, P. (2003) Polymorphism of a specific region in the gene p23 of Citrus tristeza virus allows differentiation between mild and severe isolates. Arch. Virol. 148, 2281 2291.
39. Satyanarayana, T., Gowda, S., Boyko, V.P., Albiach-Martí, M.R., Mawassi, M., Navas-Castillo, J., Karasev, A.V., Dolja, V., Hilf, M.E., Lewandowsky, D.J., Moreno, P., Bar-Joseph, M., Garnsey, S.M. Dawson, W.O. (1999) An engineered closterovirus RNA replicon and analysis of heterologous terminal sequences for replication. Proc. Natl. Acad. Sci. USA, 96, 7433 7438.
40. Satyanarayana, T., Gowda, S., Mawassi, M., Albiach-Martí, M.R., Ayllón, M.A., Robertson, C., Garnsey, S.M. Dawson, W.O. (2000) Closterovirus encoded HSP70 homolog and p61 in addition to both coat proteins function in efficient virion assembly. Virology, 278, 253 265.
41. Satyanarayana, T., Bar-Joseph, M., Mawassi, M., Albiach-Martí, M.R., Ayllón, M.A., Gowda, S., Hilf, M.E., Moreno, P., Garnsey, S.M. Dawson, W.O. (2001) Amplification of Citrus tristeza virus from a cDNA clone and infection of citrus trees. Virology, 280, 87 96.
42. Satyanarayana, T., Gowda, S., Ayllón, M.A., Albiach-Martí, M.R. Dawson, W.O. (2002a) Mutational analysis of the replication signals in the 3′-non translated region of Citrus tristeza virus. Virology, 300, 140 152.
43. Satyanarayana, T., Gowda, S., Ayllón, M.A., Albiach-Martí, M.R., Rabindram, R. Dawson, W.O. (2002b) The p23 protein of Citrus tristeza virus controls asymmetrical RNA accumulation. J. Virol. 76, 473 483.
44. Satyanarayana, T., Gowda, S., Ayllón, M.A. Dawson, W.O. (2003) Frameshift mutations in infectious cDNA clones of Citrus tristeza virus: a strategy to minimize the toxicity of viral sequences to Escherichia coli. Virology, 313, 481 491.
45. Satyanarayana, T., Gowda, S., Ayllón, M.A. Dawson, W.O. (2004) Closterovirus bipolar virion: evidence for initiation of assembly by minor coat protein and its restriction to the genomic RNA 5′ region. Proc. Natl. Acad. Sci. USA, 101, 799 804.
46. Siegel, S. Castellan, N.J. (1988) Nonparametric Statistics for the Behavioral Sciences. Singapore : McGraw Hill.
47. Tatineni, S., Robertson, C., Garnsey, S.M., Bar-Joseph, M., Gowda, S. Dawson, W.O. (2008) Three genes of Citrus tristeza virus are dispensable for infection and movement throughout some varieties of citrus. Virology, 376, 297 307.
48. Tarusova, T.A. Madden, T.L. (1999) Blast 2 sequences - a new tool for comparing protein and nucleotide sequences. FEMS Microbiol Lett. 174, 247 250.
49. Thompson, J.D., Higgins, D.G. Gibson, T.J. (1994) Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673 4680.
50. Van Vuuren, S.P., Collins, R.P. da Graça, J.V. (1993) Evaluation of citrus tristeza virus isolates for cross protection of grapefruit in South Africa. Plant Dis. 77, 24 28.
51. Vives, M.C., Rubio, L., Sambade, A., Mirkov, T.E., Moreno, P. Guerri, J. (2005) Evidence of multiple recombination events between two RNA sequence variants within a Citrus tristeza virus isolate. Virology, 331, 232 237.
52. Wallace, J.M. Drake, R.J. (1972) Studies on recovery of citrus plants from seedling yellows and the resulting protection against reinfection. In : Proceedings of the 5th Conference of the International Organization of Citrus Virologists (Price, W.C. ed.), pp. 127 136. Gainesville, FL : University of Florida Press.
53. Weng, Z., Barthelson, R., Gowda, S., Hilf, M.E., Dawson, W.O., Galbraith, D.W. Xiong, Z. (2007) Persistent infection and promiscuous recombination of multiple genotypes of an RNA virus within a single host generate extensive diversity. PLoS ONE, 2, e917.