Abstract
We estimated genetic variation in two groups of Citrus tristeza virus (CTV) isolates: one of them (isolates T385, T317, T318 and T305) derived from a Spanish source by successive host passages, and the other (isolates T388 and T390), obtained after aphid transmission of a Japanese source. The population structure of these isolates had been characterized by single-strand conformation polymorphism analysis of genes p18 and p20. The nucleotide sequences of representative haplotypes of each isolate and gene were used to estimate genetic diversity within and between isolates and to evaluate genetic differentiation between populations. Phylogenetic analysis of p18 and p20 sequence variants showed two main groups: one them included variants predominant in the severe isolates (T318, T305 and T388), and the other comprised variants present in both mild (T385, T317) and severe isolates. Most sequence variants of isolate T390 were not associated to these groups. In some isolates, within-isolate diversity was higher than diversity with other isolates because their population contained distantly related sequence variants, some of which were genetically close to variants predominant in the second isolate. Isolates T388 and T390 were genetically different for the two genes, as estimated by the F statistic. Furthermore, genetic differentiation between T385 and T317, T318 and T305 increased after each host passage. Our results suggest that aphid transmission and host passage may significantly alter the composition of CTV populations and thus be an important factor in their evolution.
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G.P. Martelli, A.A. Agranovsky, M. Bar-Joseph, D. Boscia, T. Candresse, R.H.A. Coutts, V.V. Dolja, J.E. Duffus, B.W. Falk, D. Gonsalves, V. Jelkmann, A.V. Karasev, A. Minafra, A. Murant, S. Namba, C.L. Niblett, H.J. Vetten, N. Yoshikawa, in Virus Taxonomy, 7th Report of the International Committee for Taxonomy of Viruses, ed. by M.H.V. van Regenmortel, C.M. Fauquet, D.H.L. Bishop, E.B. Carstens, M.K. Estes, S.M. Lemon, J. Maniloff, M.A. Mayo, D.J. McGeoch, C.R. Pringle, R.B. Wickner (Academic Press, San Diego, 2000), pp. 943–964
A.V. Karasev, Annu. Rev. Phytopathol. 38, 293–324 (2000)
G.P. Martelli, A.A. Agranovsky, M. Bar-Joseph, D. Boscia, T. Candresse, R.H. Coutts, V.V. Dolja, B.W. Falk, D. Gonsalves, W. Jelkmann, A.V. Karasev, A. Minafra, S. Namba, H.J. Vetten, G.C. Wisler, N. Yoshikawa, Arch. Virol. 147, 2039–2044 (2002)
V.J. Febres, L. Ashoulin, M. Mawassi, A. Frank, M. Bar-Joseph, K.L. Manjunath, R.F. Lee, C.L. Niblett, Phytopathology 86, 1331–1335 (1996)
T. Satyanarayana, S. Gowda, M.A. Ayllón, W.O. Dawson, Proc. Natl. Acad. Sci. USA 101, 799–804 (2004)
M.R. Albiach-Martí, M. Mawassi, S. Gowda, T. Satyanarayana, M.E. Hilf, S. Shanker, E.C. Almira, M.C. Vives, C. López, J. Guerri, R. Flores, P. Moreno, S.M. Garnsey, W.O. Dawson, J. Virol. 74, 6856–6865 (2000)
A.V. Karasev, V.P. Boyko, S. Gowda, O.V. Nikolaeva, M.E. Hilf, E.V. Koonin, C.L. Niblett, K. Cline, D.J. Gumpf, R.F. Lee, S.M. Garnsey, D.J. Lewandowski, W.O. Dawson, Virology 208, 511–520 (1995)
H.R. Pappu, A.V. Karasev, E.J. Anderson, S.S. Pappu, M.E. Hilf, V.J. Febres, R.M.G. Eckloff, M. Mccaffery, V. Boyko, S. Gowda, V.V. Dolja, E.V. Koonin, D.J. Gumpf, K.C. Cline, S.M. Garnsey, W.O. Dawson, R.F. Lee, C.L. Niblett, Virology 199, 35–46 (1994)
M. Mawassi, E. Mietkiewska, R. Gofman, G. Yang, M. Bar-Joseph, J. Gen. Virol. 77, 2359–2364 (1996)
M.C. Vives, L. Rubio, C. López, J. Navas-Castillo, M.R. Albiach-Martí, W.O. Dawson, J. Guerri, R. Flores, P. Moreno, J. Gen. Virol. 80, 811–816 (1999)
Z.N. Yang, D.H. Mathews, J.A. Dodds, T.E. Mirkov, Virus Genes 19, 131–142 (1999)
G. Suastika, T. Natsuaki, H. Terui, T. Kano, H. Leki, S. Okuda, J. Gen. Plant Pathol. 67, 73–77 (2001)
M.E. Hilf, A.N. Karasev, H.R. Pappu, D.J. Gumpf, C.L. Niblett, S.M. Garnsey, Virology 208, 576–582 (1995)
J. Navas-Castillo, M.R. Albiach-Martí, S. Gowda, M.E. Hilf, S.M. Garnsey, W.O. Dawson, Virology 228, 92–97 (1997)
M.A. Ayllón, T. Satyanarayana, S. Gowda, W.O. Dawson, Mol. Plant Pathol. 6, 165–176 (2005)
T. Satyanarayana, S. Gowda, V.P. Boyko, M.R. Albiach-Martí, M. Mawassi, J. Navas-Castillo, A.V. Karasev, V. Dolja, M.E. Hilf, D.J. Lewandowski, P. Moreno, M. Bar-Joseph, S.M. Garnsey, W.O. Dawson, Proc. Natl. Acad. Sci. USA 96, 7433–7438 (1999)
T. Satyanarayana, S. Gowda, M. Mawassi, M.R. Albiach-Martí, M.A. Ayllón, C. Robertson, S.M. Garnsey, W.O. Dawson, Virology 278, 253–265 (2000)
S. Gowda, T. Satyanarayana, C.L. Davis, J. Navas-Castillo, M.R. Albiach-Martí, M. Mawassi, N. Valkov, M. Bar-Joseph, P. Moreno, W.O. Dawson, Virology 274, 246–254 (2000)
C. López, J. Navas-Castillo, S. Gowda, P. Moreno, R. Flores, Virology 269, 462–470 (2000)
S. Gowda, T. Satyanarayana, M.A. Ayllón, M.R. Albiach-Martí, M. Mawassi, S. Rabindran, SM. Garnsey, W.O. Dawson, Virology 286, 134–151 (2001)
R. Lu, A. Folimonov, M. Shintaku, W.-X. Li, B.W. Falk, W.O. Dawson, S.W. Ding, Proc. Natl. Acad. Sci. USA 101, 15742–15747 (2004)
R. Ghorbel, C. López, C. Fagoaga, P. Moreno, L Navarro, R. Flores, L. Peña, Mol. Plant Pathol. 2, 27–36 (2001)
C. Fagoaga, C. López, P. Moreno, L. Navarro, R. Flores, L. Peña, Mol. Plant Microbe Interact. 18, 435–445 (2005)
J.F. Ballester-Olmos, J.A. Pina, L. Navarro, in Proc. 10th Conf. Int. Organ Citrus Virol., ed. by L.W. Timmer, S.M. Garnsey, L. Navarro (IOCV, Riverside, CA, 1988), pp. 28–32
J.F. Ballester-Olmos, J.A. Pina, E. Carbonell, P. Moreno, A. Hermoso de Mendoza, M. Cambra, L. Navarro, Plant Pathol. 42, 219–229 (1993)
A. Hermoso de Mendoza, J.F. Ballester-Olmos, J.A. Pina, in Proc. 10th Conf. Int. Organ Citrus Virol., ed. by L.W. Timmer, S.M. Garnsey, L. Navarro (IOCV, Riverside, CA, 1988), pp. 68–70
P. Moreno, J. Guerri, J.F. Ballester-Olmos, R. Albiach, M.E. Martínez, Plant Pathol. 42, 3541 (1993)
P. Moreno, J. Guerri, J.F. Ballester-Olmos, C. Fuertes-Polo, R. Albiach, M.E. Martínez, in Proc. 12th Conf. Int. Organ Citrus Virol., ed. by P. Moreno, J.V. da Graça, L.W. Timmer (IOCV, Riverside, CA, 1993), pp. 8–15
C.N. Roistacher, P. Moreno, in Proc. 11th Conf. Int. Organ Citrus Virol., ed. by R.H. Brlansky, R.F. Lee, L.W. Timmer (IOCV, Riverside, CA, 1991), pp. 7–19
T. Kano, M. Koizumi, in Proc 11th Conf Int Organ Citrus Virol., ed. by R.H. Brlansky, R.F. Lee, L.W. Timmer (IOCV, Riverside, CA, 1991) pp. 82–85
P. Moreno, J. Guerri, N. Muñoz, Phytopathology 80, 477–482 (1990)
P. Moreno, J. Guerri, J.F. Ballester-Olmos, M.E. Martínez, in Proc. 11th Conf. Int. Organ Citrus Virol., ed. by R.H. Brlansky, R.F. Lee, L.W. Timmer (IOCV, 7Riverside, CA, 1991), pp. 20–24
M.R. Albiach-Martí, J. Guerri, A. Hermoso de Mendoza, F. Laigret, J.F. Ballester-Olmos, P. Moreno, Phytopathology 90, 134–138 (2000)
M.A. Ayllón, C. López, J. Navas-Castillo, S.M. Garnsey, J. Guerri, R. Flores, P. Moreno, Arch. Virol. 146, 27–40 (2001)
P. Kong, L. Rubio, M. Polek, B.W. Falk, Virus Genes 21, 139–145 (2000)
C. López, M.A. Ayllón, J. Navas-Castillo, J. Guerri, P. Moreno, R. Flores, Phytopathology 88, 685–691 (1998)
L Rubio, M.A. Ayllón, P. Kong, A. Fernández, M. Polek, J. Guerri, P. Moreno, B.W. Falk, J.Virol. 75, 8054–8062 (2001)
A. Roy, R.H. Brlansky, Arch. Virol. 149, 1911–1929 (2004)
E. Domingo, J.J. Holland in The Evolutionary Biology of Viruses, ed. by S.S. Morse (Raven Press, New York, 1994), pp. 161–184
R.H. Brlansky, V.D. Damsteegt, D.S. Howd, A. Roy, Plant Dis. 87, 397–401 (2003)
A. Sambade, C. López, L. Rubio, R. Flores, J. Guerri, P. Moreno, Arch. Virol. 148, 2281–2291 (2003)
M.A. Ayllón, S. Gowda, T. Satyanarayana, W.O. Dawson, Virology 322, 41–50 (2004)
M.C. Vives, L. Rubio, A. Sambade, T.E. Mirkov, P. Moreno, J. Guerri, Virology 331, 232–237 (2005)
M.A. Ayllón, L. Rubio, A. Moya, J. Guerri, P. Moreno, Virology 255, 32–39 (1999)
J. Sambrook, E.F. Fritsch, T. Maniatis, Molecular Cloning. A laboratory Manual (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NewYork 1989)
J.D. Thompson, D.G. Higgins, T.J. Gibson, Nucleic Acids Res. 22, 4673–4680 (1994)
S. Kumar, K. Tamura, I.B. Jakobsen, M. Nei, Bioinformatics 17, 1244–1245 (2001)
P. Pamilo, N.O. Bianchi, Mol. Biol. Evol. 10, 271–281 (1993)
W.H. Li, J. Mol. Evol. 36, 96–99 (1993)
J. Felsenstein, PHYLIP (Phylogeny Inference Package) Version 3.6., Distributed by the author (Department of Genome Sciences, University of Washington, Seattle, 2004)
B.S. Weir, C.C. Cockerham, Evolution 38, 1358–1370 (1984)
M.C. Vives, L. Rubio, L. Galipienso, L. Navarro, P. Moreno, J. Guerri, J. Gen. Virol. 83, 2587–2591 (2002)
M.A. Bracho, A. Moya, E. Barrio, J. Gen. Virol. 79, 2921–2928 (1998)
F. D’Urso, M.A. Ayllón, L. Rubio, A. Sambade, A. Hermoso de Mendoza, J. Guerri, P. Moreno, Plant Pathol. 49, 288–294 (2000)
L. Rubio, J. Soong, J. Kao, B.W. Falk, Phytopathology 89, 707–711 (1999)
L Rubio, Y. Abou-Jawdah, H. Lin, B.W. Falk, J. Gen. Virol. 82, 929–933 (2001)
F. García-Arenal, A. Fraile, J.M. Malpica, Annu. Rev. Phytopathol. 39, 157–186 (2001)
W.L. Schneider, M.J. Roossinck, J. Virol. 75, 6566–6571 (2001)
S. Sacristán, J.M. Malpica, A. Fraile, F. García-Arenal, J. Virol. 77, 9906–9911 (2003)
E. Rodriguez-Cerezo, S.F. Elena, A. Moya, F. García-Arenal, J. Mol. Evol. 32, 328–332 (1991)
E. Rodriguez-Cerezo, F. García-Arenal, Virology 170, 418–423 (1989)
A. Sambade, L. Rubio, S.M. Garnsey, N. Costa, G.W. Müller, M. Peyrou, J. Guerri, P. Moreno, Plant Pathol. 51, 257–265 (2002)
M.A. Ayllón, C. López, J. Navas-Castillo, M. Mawassi, W.O. Dawson, J. Guerri, R. Flores, P. Moreno, J. Gen. Virol. 80, 817–821 (1999)
G. Yang, X. Che, R. Gofman, Y. Ben Shalom, D. Piestun, R. Gafny, M. Mawassi, M. Bar-Joseph, Virus Genes 19, 5–13 (1999)
Acknowledgments
We are indebted to M.E. Martínez and M. Boil for technical assistance in the laboratory. We thank Dr. Jaime Cubero for his critical review of the manuscript. First and second authors were recipients of doctoral fellowships from the CICYT and the Conselleria de Cultura, Educación y Ciencia de la Generalitat Valenciana, respectively. This work was supported by projects SC 93-111 (INIA), AGL2001-1973 (DGCYT), AGL2004-05099/AGR and BMC2001-3096 (MCYT) and by grant to I+D+I groups GRUPOS03/221 from the Generalitat Valenciana.
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Ayllón, M.A., Rubio, L., Sentandreu, V. et al. Variations in Two Gene Sequences of Citrus Tristeza Virus after Host Passage. Virus Genes 32, 119–128 (2006). https://doi.org/10.1007/s11262-005-6866-4
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DOI: https://doi.org/10.1007/s11262-005-6866-4