Abstract
Prevalence of citrus tristeza virus (CTV) isolates causing severe stem pitting symptoms with a high diverse genetic composition represents a threat for citrus crops in Uruguay. This work aimed to characterize viral components of CTV populations segregated by single aphid (Toxoptera citricida) transmission (SAT). Thirty-nine SAT-derived sub-isolates were obtained from six CTV field isolates. Only eight were MCA13 non-reactive, and six of them, together with other three MCA13 reactive sub-isolates, were considered mild by the intensity of their reaction in ‘Mexican’ lime, ‘Madam Vinous’ sweet orange, ‘Duncan’ grapefruit and sour orange indicator plants. Fourteen sub-isolates, including two MCA13 non-reactive, were considered moderate, and the remaining sub-isolates were all MCA13 reactive and with severe reactions in the indicator plants. Sequence comparisons of the p20, p23 and p25 genes showed a high inter (among all isolates and their derived sub-isolates)- and intra (among each isolate and its derived sub-isolates)-specific evolutionary diversity, with the presence of the CTV strains VT, T3, RB, and NC in mixtures of their complex populations. Together, our data revealed the heterogeneity of the Uruguayan CTV populations in these CTV field isolates. The results provide additional biological and molecular information on the complex CTV populations in Uruguay and must be considered for improving the CTV management program.



Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Akaike H (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19:716–723
Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Systematic Biology 55:539–552
Arruabarrena A, Benítez-Galeano MJ, Giambiasi M, Bertalmío A, Colina R, Hernández-Rodríguez L (2016) Application of a simple and affordable protocol for isolating plant total nucleic acids for RNA and DNA virus detection. Journal of Virological Methods 237:14–17
Ayllón MA, Rubio L, Moya A, Guerri JA, Moreno P (1999) The haplotype distribution of two genes of citrus tristeza virus is altered after host change or aphid transmission. Virology 255:32–39
Bar-Joseph M, Loebenstein G (1973) Effects of strain, source plant, and temperature on the transmissibility of citrus tristeza virus by the melon aphid. Phytopathology 63:716–720
Bar-Joseph M, Marcus R, Lee RF (1989) The continuous challenge of citrus tristeza virus control. Annual Review of Phytopathology 27:291–316
Benítez-Galeano MJ, 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. Viruses 7:4152–4168
Benítez-Galeano MJ, Vallet T, Carrau L, Hernández-Rodríguez L, Bertalmío A, Rivas F, Rubio L, Maeso D, Vignuzzi M, Moratorio G, Colina R (2018) Complete genome sequence of a novel recombinant citrus tristeza virus, a resistance-breaking isolate from Uruguay. Genome Announcements 6:e00442–e00418
Brlansky RH, Damsteegt VD, Howd DS, Roy A (2003) Molecular analyses of citrus tristeza virus subisolates separated by aphid transmission. Plant Disease 87:397–401
Broadbent P, Brlansky RH, Indsto J (1996) Biological characterization of Australian isolates of citrus tristeza virus and separation of subisolates by single aphid transmission. Plant Disease 80:329–333
Calavan EC, Harjung MK, Blue RL, Roistacher CN, Gumpf DJ, Moore PW (1980) Natural spread of seedling yellows and sweet orange and grapefruit stem pitting tristeza viruses at the University of California, Riverside. In: Proceedings of the 8th Conference of the International Organization of Citrus Virologists. IOCV, Riverside. pp 69–75
Cambra M, Garnsey SM, Permar TA, Henderson CT, Gumpf DJ, Vela C (1990) Detection of citrus tristeza virus (CTV) with a mixture of monoclonal antibodies. Phytopathology 80:103
Dawson WO, Bar-Joseph M, Garnsey SM, Moreno P (2015) Citrus tristeza virus: making an ally from an enemy. Annual Review of Phytopathology 53:137–155
Folimonova S (2013) Developing an understanding of cross-protection by citrus tristeza virus. Frontiers in Microbiology 4:76
Garnsey SM, Gumpf DJ, Roistacher CN, Civerolo EL, Lee RF, Yokomi RK, Bar-Joseph M (1987) Toward a standardized evaluation of the biological properties of citrus tristeza virus. Phytophylactica 19:151–157
Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52:696–704
Guindon S, Dufayard J, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: 3.0. Systematic Biology 59:307–321
Hall TA (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 SJ (2013) Citrus tristeza virus: evolution of complex and varied genotypic groups. Frontiers in Microbiology 4:93
Harper SJ, Cowell SJ, Dawson WO (2015a) Finding balance: virus populations reach equilibrium during the infection process. Virology 485:205–212
Harper SJ, Cowell SJ, Dawson WO (2015b) With a little help from my friends: complementation as a survival strategy for viruses in a long-lived host system. Virology 478:123–128
Hernández-Rodríguez L, Bertalmío A, Arruabarrena A, Rubio L, Rivas F, Benítez-Galeano MJ, Colina R, Maeso D (2017) First report of the citrus tristeza virus trifoliate resistance-breaking (RB) genotype in 'Newhall' sweet orange in South America. Plant Disease 101:1
Koch de Brotos L, Boasso C (1955) Lista de las enfermedades de los vegetales en el Uruguay. Ministerio de Ganadería y Agricultura, Montevideo
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33:1870–1874
Lin Y, Brlansky RH, Powell CA (2002) Inefficient transmission of citrus tristeza virus from grapefruit by single brown citrus aphids. Hortscience 37:936–939
Moreno P, Ambros S, Albiach-Martí MR, Guerri J, Peña L (2008) Citrus tristeza virus: a pathogene that changed the course of the citrus industry. Molecular Plant Pathology 9:251–268
Permar TA, Garnsey SM, Gumpf DJ, Lee RT (1990) A monoclonal antibody that discriminates strains of citrus tristeza virus. Phytopathology 80:224–228
Posada D (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25:1253–1256
Roistacher CN (1991) Graft-transmissible diseases of Citrus. Handbook for detection and diagnosis. FAO, Rome
Roistacher CN, Nauer EM, Kishaba A, Calavan EC (1980) Transmission of citrus tristeza virus by Aphis gossypii reflecting changes in virus transmissibility in California. In: Proceedings of the 8th Conference of the International Organization of Citrus Virologists. IOCV, Riverside. pp 76–82
Roistacher CN, da Graça JV, Müller GW (2010) Cross protection against citrus tristeza virus - a review. In: Hilf ME, Timmer LW, Milne RG, da Graça JV (Eds.) Proceeding of the 17th Conference of the International Organization of Citrus Virology. IOCV, Riverside. pp. 1–27
Roy A, Brlansky RH (2009) Population dynamics of a Florida citrus tristeza virus isolate and aphid-transmitted sub-isolates: identification of three genotypic groups and recombinants after aphid transmission. Phytopathology 99:1297–1306
Rubio L, Bertalmío A, Hernández-Rodríguez L, Benítez Galeano MJ, Arruabarrena A, Rivas F, Colina R, Maeso D (2019) Biological and molecular characterization of Uruguayan citrus tristeza virus field isolates. Journal of Plant Pathology 101:97–105
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 148:2325–2340
Timmer LW, Garnsey SM, Graham JH (2000) Compendium of citrus diseases. APS Press, St Paul
Yokomi RK, Polek M, Gumpf DJ (2010) Transmission and spread of citrus tristeza virus in central California. In: Karasev AV, Hilf ME (Eds). Citrus tristeza virus complex and tristeza diseases. APS Press, St. Paul. pp. 151–165
Yokomi RK, Selvaraj V, Maheshwari Y, Saponari M, Giampetruzzi A, Chiumenti M, Hajeri S (2017) Identification and characterization of citrus tristeza virus isolates breaking resistance in trifoliate orange in California. Phytopathology 107:901–908
Zhou CY, Wang XF, Liu YQ, Liu KH, Zou Q, Xiang Y, Li ZA (2011) Influence of the quantity and variability of citrus tristeza virus on transmissibility by single Toxoptera citricida. Journal of Plant Pathology 93:97–103
Acknowledgments
This research was funded by the Instituto Nacional de Investigación Agropecuaria (INIA), Uruguay (project CT-06), through the National Program of Citrus Research and the National Citrus Sanitation Program.
Author information
Authors and Affiliations
Corresponding author
Additional information
Section Editor: Juliana Freitas-Astua
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hernández-Rodríguez, L., Benítez-Galeano, M.J., Bertalmío, A. et al. Diversity of Uruguayan citrus tristeza virus populations segregated after single aphid transmission. Trop. plant pathol. 44, 352–362 (2019). https://doi.org/10.1007/s40858-019-00288-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40858-019-00288-x


