Abstract
Citrus tristeza virus (CTV) causes various syndromes of citrus and consists of diverse strains which may cause symptoms of differing severity. Lemon is the most important citrus crop produced in Tucumán province, Argentina, but the diversity of CTV strains within this region has been poorly studied. In this study we identified strains of CTV in lemons in 29 trees of five commonly planted lemon cultivars from this area using direct Sanger and next generation sequencing (NGS) of amplicons derived from the CTV p33 gene. The Kpg3/SP/T3 genotype was dominant in 28 of the 29 samples analysed, with one sample being dominant for a genotype of RB. This was confirmed with NGS in all but one instance. In addition, all thirteen samples tested by NGS were infected with RB, Kpg3/SP/T3 and HA 16–5 genotypes. One sample also had a minor VT component, while a further two samples also had a minor AT-1 component.
References
Bar-Joseph, M., Marcus, R., & Lee, R. F. (1989). The continuous challenge of citrus tristeza virus control. Annual Review of Phytopathology, 27, 291–316.
Benítez-Galeano, M. J., Rubio, L., Bertalmío, A., Maeso, D., Rivas, F., & Colina, R. (2015). Phylogenetic studies of the three RNA silencing suppressor genes of South American CTV isolates reveal the circulation of a novel genetic lineage. Virus, 7, 4152–4168. doi:10.3390/v7072814.
Besoain, X., Bertolini, E., Camps, R., Ramella, F., Gorris, M. T., Torres, M., & Cambra, M. (2015). Aggressive Citrus tristeza virus isolates in Chile are MCA13-positive and VT type, while mild isolates are MCA13-negative and T30 type. Ciencia e Investigación Agraria, 42(2), 251–262.
Broadbent, P., Bevington, K., Fraser, L., & Freeman, B. (1980). Behavior of Citrus macrophylla as a rootstock for Eureka lemon in trials in new South Wales. In Proceedings of the 8th Conference of the International organisation of citrus Virologists (pp. 40–43). Riverside: IOCV.
Broadbent, P., Brlansky, R. H., & Indsto, J. (1996). Biological characterization of Australian isolates of citrus tristeza virus and separation of subisolates by single aphid transmission. Plant Disease, 80(3), 329–333.
Calavan, E., & Burns, R. N. (1968). Tristeza in lemon on Citrus macrophylla rootstock. Citrograph, 53, 108–122.
Cordas, D. (1975). Tristeza found on Lisbon lemon in San Joaquin. Citrograph, 60, 368.
Dawson, W. O., Garnsey, S. M., Tatineni, S., Folimonova, S. Y., Harper, S. J., & Gowda, S. (2013). Citrus tristeza virus-host interactions. Frontiers in Microbiology, 4(Article 88), 1–10.
Figueroa, J., Foguet, L., Figueroa Castellanos, A. I., & Stein, B. (2009). Biological characterization of citrus tristeza virus strains in lemon in Tucuman, Argentina. Revista Industrial y Agricola de Tucuman, 86(1), 37–41.
Figueroa, J., Foguet, L., Escobar Ponce De Leon, C., Palalcios, F., Martos, G., & Stein, B. (2012). Natural spread of Citrus tristeza virus in lemon varieties. Revista Industrial y Agrícola de Tucumán, 89(1), 43–46.
Foguet, J. L. (1961). Presencia del virus de la tristeza de los citrus en Tucuman. IDIA, Suplemento, 6, 80–84.
Foguet, J. L., Gonzalez, J. L., Vinciguerra, H., & Stein, B. (1987). Ensayo de portainjertos para limonero Genova EEAT nuc en un suelo de replante. Revista Industrial y Agricola de Tucuman, 64(2), 43–54.
Folimonova, S. Y. (2012). Superinfection exclusion is an active virus-controlled function that requires a specific viral protein. Journal of Virology, 86, 5554–5561.
Folimonova, S. Y., Robertson, C. J., Shilts, T., Folimonov, A. S., Hilf, M. E., Garnsey, S. M., & Dawson, W. O. (2010). Infection with strains of citrus tristeza virus does not exclude superinfection by other strains of the virus. Journal of Virology, 84, 1314–1325.
Garnsey, S. M., Gumpf, D. J., Roistacher, C. N., Civerolo, E. L., Lee, R. F., Yokomi, R. K., & Bar-Joseph, M. (1987). Toward a standardized evaluation of the biological properties of citrus tristeza virus. Phytophylactica, 19(2), 151–157.
Garnsey, S. M., Civerolo, D. J., Gumpf, R. K., Yokomi, R. K., & Lee, R. F. (1991). Development of a worldwide collection of CTV isolates. In R. H. Brlansky, R. F. Lee, & L. W. Timmer (Eds.), Proceedings of the 11th Conference of the International Organization of Citrus Virologists (pp. 113–120). Riverside: IOCV.
Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
Harper, S. J. (2013). Citrus tristeza virus: Evolution of complex and varied genotypic groups. Frontiers in Microbiology, 4, 93.
Harper, S.J., & Pearson, M.N. (2015). Citrus tristeza virus strains present in New Zealand and the South Pacific. Journal of Citrus Pathology, 2 iocv_journalcitruspathology_#27580. pp 1-5.
Herrera, M. G., Madariaga, M., & Santalices, M. (1995). Detección del virus de la tristeza de los cítricos, CTV en el valle central de Chile. Agricultura Técnica (Chile), 55(2), 167–169.
Hilf, M. E., Mavrodieva, V. A., & Garnsey, S. M. (2005). Genetic marker analysis of a global collection of a Citrus tristeza virus: Characterization and distribution of CTV genotypes and association with symptoms. Phytopathology, 95, 909–917.
Mc Clean, A. P. D. (1950). Remove from marked records virus infections of citrus in South Africa, III. Stem-pitting disease of grapefruit. Farming in South Africa, 25(294), 289–296.
Moreno, P., Ambrós, S., Albiach-Martí, M. R., Guerri, J., & Peña, L. (2008). Citrus tristeza virus: A pathogen that changed the course of the citrus industry. Molecular Plant Pathology, 9(2), 251–268.
Palacios, M. F., Figueroa, J., Foguet, L., Escobar, C., & Stein, B. (2013). Molecular identification of CTV genotypes from northwestern Argentina. In Proceedings of the 19th Conference of the International Organization of Citrus Virologists (p. 26). Riverside: IOCV.
Piquer, J., Pina, J. A., Perez-Panades, J., Carbonell, E. A., Guerra, J., & Moreno, P. (2005). Preliminary evaluation of the sensitivity of Alemow rootstock to Citrus tristeza virus in Spain. In Proceedings of the 16th Conference of the International Organization of citrus Virologists (pp. 94–99). Riverside: IOCV.
Read, D. A., & Pietersen, G. (2015). Genotypic diversity of citrus tristeza virus within red grapefruit, in a field trial site in South Africa. European Journal of Plant Pathology, 142(3), 531–545.
Read, D. A., & Pietersen, G. (2016a). PCR bias associated with conserved primers designed to determine genotype diversity within citrus tristeza virus populations. Journal of Virological Methods, 237, 107–113.
Read, D. A., & Pietersen, G. (2016b). Diversity of citrus tristeza virus populations in commercial grapefruit orchards in southern Africa, determined using Illumina MiSeq technology. Eur J Plant Pathol. doi:10.1007/s10658-016-1096-2.
Roy, A., Ananthakrishnan, G., Hartung, J. S., & Brlansky, R. H. (2010). Development and application of a multiplex reverse-transcription polymerase chain reaction assay for screening a global collection of citrus tristeza virus isolates. Phytopathology, 100, 1077–1088.
Sambade, A., López, C., Rubio, L., Flores, R., Guerri, J., & Moreno, P. (2003). Polymorphism of a specific region in gene p23 of citrus tristeza virus allows discrimination between mild and severe isolates. Archives of Virology, 148(12), 2325–2340.
Sambrook, J. (2001). Molecular cloning: ‘a laboratory manual’. New York: Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
Scott, K. A., Hlela, Q., Zablocki, O., Read, D. A., Van Vuuren, S. P., & Pietersen, G. (2013). Genotype composition of populations of Citrus tristeza virus grapefruit cross-protecting GFMS12 in different host plants and aphid-transmitted sub-isolates. Archives of Virology, 158(1), 27–37.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.
Van Vuuren, S. P. (2002). Effects of citrus tristeza virus isolates on two tolerant commercial scions on different rootstocks in South Africa. In Proceedings of the 15th Conference of the International Organization of Citrus Virologists. (Duran-Vila, N., Milne, R.G., & da Graça, J.V.) (pp. 31–38). Riverside: IOCV.
Varveri, C., Olmos, A., Pina, J. A., Marroquin, C., & Cambra, M. (2015). Biological and molecular characterization of a distinct citrus tristeza virus isolate originating from a lemon tree in Greece. Plant Pathology, 64(4), 792–798.
van Vuuren, S. P., & Manicom, B. Q. (2005). The response of star ruby grapefruit to different citrus tristeza virus isolates. In M. E. Hilf, N. Duran-Vila, & M. A. Rocha-Peña (Eds.), Proceedings of the 16th Conference of the International Organization of Citrus Virologists (pp. 112–116). Riverside: IOCV.
Weathers, L., & Sánchez, L. (1970). Tristeza disease of citrus in Chile. Plant Dis Rep, 54, 542–544.
Zeman, V. (1931). Una enfermedad nueva en los naranjales de Corrientes. Physis, 19, 410–411.
Acknowledgements
We would like to acknowledge funding from the National Research Foundation (South Africa) and Ministerio de Ciencia, Tecnologia e Innovación Productiva (Argentina) via the South Africa-Argentina Bilateral agreement programme.
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Read, D.A., Palacios, M.F., Figueroa, J. et al. Survey of citrus tristeza virus (CTV) strains in Citrus x limon (L) Burm f. (lemon) in Tucumán Province, Argentina. Eur J Plant Pathol 149, 1029–1039 (2017). https://doi.org/10.1007/s10658-017-1245-2
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DOI: https://doi.org/10.1007/s10658-017-1245-2