Articles
Genotype variation of citrus tristeza virus after passage on different hosts, and changes in the virus genotype populations by the vector Aphis gossypii
Nicola Fiore- Natalia Riquelme
- Wilson Barros-Parada
- Ximena Besoain
Published 2022-03-25
Keywords
- Citrus sinensis,
- Citrus aurantifolia,
- mild CTV isolates,
- VT genotype
How to Cite
[1]
R. Camps, N. Fiore, N. Riquelme, W. Barros-Parada, and X. Besoain, “Genotype variation of citrus tristeza virus after passage on different hosts, and changes in the virus genotype populations by the vector Aphis gossypii”, Phytopathol. Mediterr., vol. 61, no. 1, pp. 55–63, Mar. 2022.
Abstract
Phylogenetic analyses categorize seven genotypes of citrus tristeza virus (CTV). The symptoms caused by this pathogen, their expression and severity are influenced by CTV genotypes, host species, cultivars, and infected host rootstocks. This study aimed to verify how populations of Chilean CTV isolates changed following inoculation from infected sweet orange to Mexican lime trees, and to determine if CTV genotype populations influenced transmission efficiency via Aphis gossypii. Reverse transcription polymerase chain reaction showed variation in genotypes of populations of CTV in Mexican lime, after graft inoculations using infected sweet orange chip-buds. Severe genotypes (VT) were detected after inoculation of mild isolate CTV populations (T30). The T30 donor populations also reduced transmissibility via A. gossypii; however, these results may not be conclusive due to mixture with the VT genotype. There is evidence of high rates of virus acquisition by this aphid species, but also low transmission efficiency, which may partially explain the historical absence of tristeza epidemics in Chile.
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References
Albiach-Martí M.R., Mawassi M., Gowda S., Satyanarayana T., Hilf M., … Dawson W., 2000. Sequences of Citrus tristeza virus separated in time and space are essentially identical. Journal of Virology 74: 6856-6865.listo
Albiach-Martí M.R., Robertson C., Gowda S., Tatineni S., Belliure B., … Dawson W.O., 2010. 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 11: 55–67.
Bar-Joseph M., 1978. Cross-protection incompleteness: A possible cause for natural spread of Citrus tristeza virus after a prolonged lag period in Israel. Phytopathology 68: 1110-1111.
Bar-Joseph M., Marcus R., Lee R.F., 1989. The continuous challenge of Citrus tristeza virus control. Annual Review of Phytopathology 27: 291-316.
Bertolini E., Moreno A., Capote N., Olmos A., Vidal A., Pérez J., Cambra M., 2008. Quantitative detection of Citrus tristeza virus in plant tissues and single aphids by real-time RT-PCR. European Journal of Plant Pathology 120: 177-188.
Besoain X., 2008. Incidencia, caracterización y epidemiologia del virus de la tristeza de los cítricos en Chile. Tesis Doctoral, Universidad Politécnica de Valencia, Valencia, España, 129 pp.
Besoain X., Bertolini E., Camps R., Ramella F., Gorris M.T., Torres M. and 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: 251-262.
Blackman R.L. and V.F. Eastop, 2006. Aphids on the World’s herbaceous Plants and Shrubs. An Identification and Information Guide. John Wiley and Sons & The Natural History Museum. Chichester (United Kingdom). 2 vols., 1024 pp.
Brlansky R., Damsteegt V., Howd D. and Roy A., 2003. Molecular analyses of Citrus tristeza virus sub-isolates separated by aphid transmission. Plant Disease 87: 397-40.
Cambra M., Gorris M.T., Marroquín C., Román M., Olmos A., … Navarro L., 2000. Incidence and epidemiology of Citrus tristeza virus in the Valencian Community of Spain. Virus Research 71: 85-95.
Chen A., Watanabe S., Yokomi R. and Ng J.C.K., 2018. Nucleotide heterogeneity at the terminal ends of the genomes of two California Citrus tristeza virus strains and their complete genome sequence analysis. Virology Journal 15: 141.
Dawson W., Bar-Joseph M., Garsney S. and Moreno P., 2015.Citrus tristeza virus making an ally from an enemy. Annual Review of Phytopathology 53: 137-155.
Dawson W., Garnsey S., Tatineni S., Folimonova S., Harper S., Gowda S., 2013. Citrus tristeza virus-host interactions. Frontiers in Microbiology 88: 1-10.
D'urso F., Ayllon M., Rubio L., Sambade A., Hermoso de Mendoza A., Guerri J., Moreno P, 2000. Contribution of uneven distribution of genomic RNA variants of Citrus tristeza virus (CTV) within the plant to changes in the viral population following aphid transmission. Plant Pathology 49: 288-294.
Folimonova S., Robertson C., Shilts T., Folimonov A., Hilf M., Garnsey S., 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.
Fuller S., Chavigny P., Lapchin L., Vanlerberghe-Masutti F., 1999. Variation in clonal diversity in glasshouse infestations of the aphid, Aphis gossypii Glover in southern France. Molecular Ecology 8: 1867-1877.
Garnsey, S.M., Gumpf, D.J., Roistacher, C.N., Civerolo, E.L., Lee, R.F., Yokomi, R.K. and Bar-Joseph, M. 1987. Toward standardized evaluation of the biological properties of citrus tristeza virus. Phytophylactica 19:151-157.
Harper S., 2013. Citrus tristeza virus: evolution of complex and varied genotypic groups. Frontiers in Microbiology 93: 1-18.
Harper S., Dawson T., Pearson M., 2010. Isolates of Citrus tristeza virus that overcome Poncirus trifoliate resistance comprise novel strain. Archives of Virology 155: 471-480.
Harper S., Cowell S., Dawson W.O., 2015. Finding balance: Virus populations reach equilibrium during the infection process. Virology 485: 205–212.
Harper S.J., Cowell S.J., Dawson W.O., 2018. Bottlenecks and complementation in the aphid transmission of Citrus tristeza virus populations. Archives of Virology 163: 3373:3376.
Harper S., Cowell S., Robertson C., Dawson W., 2014. Differential tropism in roots and shoots infected by Citrus tristeza virus. Virology 460: 91-99.
Harper S.J., Killiny N., Tatineni S., Gowda S., Cowell S.J., Shilts T., Dawson W.O, 2016. Sequence variation in two genes determines the efficacy of transmission of Citrus tristeza virus by the brown citrus aphid. Archives of Virology 161: 3555-2559.
Hermoso de Mendoza A., Ballester-Olmos J., Pina J., 1984. Transmission of Citrus tristeza virus by aphids (Homoptera, Aphididae) in Spain. Proceedings of the 9th Conference of International Organization of Citrus Virologists (IOCV). IOCV, Riverside, CA, USA, 23-27.
Hilf M., Mavrodieva A., Garnsey S., 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.
Karasev, A. 2000. Genetic diversity and evolution of Closterovirus. Annual Review Phytopathology 38: 293-324.
Marroquín C., Olmos A., Gorris M.T., Bertolini E., Martínez M.C., … Cambra M., 2004. Estimation of the number of aphids carrying Citrus tristeza virus that visit adult citrus trees. Virus Research 100: 101-108.
Mawassi M., Gafny R., Bar-Joseph M., 1993. Nucleotide sequence of the coat protein gene of Citrus tristeza virus: comparison of biologically diverse isolates collected in Israel. Virus Genes 7: 265–275.
Melzer M.J., Borth W.B., Sether D.M., Ferreira S., Gonsalves D., Hu J., 2010. Genetic diversity and evidence for recent modular recombination in Hawaiian Citrus tristeza virus. Virus Genes 40: 111-118.
Moreno P., Ambros S., Albiach-Martí M., Guerri J., Pena L., 2008. Citrus tristeza virus: a pathogen that changed the course of the citrus industry. Molecular Plant Pathology 9: 251–268.
Nieto J.M., Fuentes-Contreras E., Castro M., Aldea M., Oretego J., Mier M.P., 2016. Catálogo de los áfidos (Hemiptera, Aphididae) de Chile, con plantas hospedadoras y distribuciones regional y provincial. Graellsia 72: 167.
Pappu H., Pappu S., Manjunath K., Lee R., Niblett C., 1993. Molecular characterization of a structural epitope that is largely conserved among severe isolates of a plant virus. Proceedings of the National Academy of Sciences of the USA 90: 3641-3644.
Permar T., Garnsey S., Gumpf D., Lee R., 1990. A monoclonal antibody that discriminates strains of Citrus tristeza virus. Phytopathology 80: 224- 228.
Rocha-Peña M., Lee R., Lastra R., Niblett C., Ochoa-Corona F., Garnsey S., Yokomy R., 1995. Citrus tristeza virus and its aphid vector Toxoptera citricida. Threats of citrus production in the Caribbean and Central and North America. Plant Disease 79: 437-445.
Roy A., Brlansky H., 2009. Population dynamics of a Florida Citrus tristeza virus isolate and aphid-transmitted subisolates: Identification of three genotypic groups and recombinants after aphid transmission. Phytopathology 99: 1297-1306.
Rubio L., Ayllón M.A., Kong P., Fernández A., Polek M., … Falk B.W., 2001. Genetic variation of Citrus tristeza virus isolates from California and Spain: evidence for mixed infections and recombinations. Journal of Virology 75: 8054-8062.
Satyanarayana T., Gowda S., Ayllón M.A., Albiach-Martí M.R., Dawson W.O., 2002. Mutational analysis of the replication signals in the 3′-nontranslated region of Citrus tristeza virus. Virology 300: 140–52.
Schneider W., Roossinck M., 2001. Genetic diversity in RNA virus quasispecies is controlled by host-virus interactions. Journal of Virology 75: 12165-12173.
Scott K., Hlela Q., Zablocki O., Read D., Vuuren S., Pietersen G., 2013. Genotype composition of populations of grapefruit-crossprotecting Citrus tristeza virus strain GFMS12 in different host plants and aphid-transmitted sub-isolates. Archives of Virology 158: 27–37.
Simbaqueba R., Serna F., Posada-Flórez F., 2014. Curaduría, Morfología e identificación de áfidos (Hemiptera: Aphididae) del museo entomológico UNAB. Primera aproximación. Boletín científico museo historia natural. 18:222-246.
Weathers L., Sánchez L., Platt G. 1969. Naturaleza y distribución de las enfermedades virosas de cítricos en Chile. Agricultura Técnica (Chile) 29:166-170.
Yokomi R.K., Selvaraj V., Maheshwari Y., Chiumenti M., Saponari M., ... Hajeri S., 2018. Molecular and biological characterization of a novel mild strain of Citrus tristeza virus in California. Archives of Virology 163: 1795-1804.
Yokomi R.K., DeBorde R.L, 2005. Incidence, transmissibility, and genotype analysis of Citrus tristeza virus (CTV) isolates from CTV eradicative and noneradicative districts in central California. Plant Disease 89: 859-866.
Albiach-Martí M.R., Robertson C., Gowda S., Tatineni S., Belliure B., … Dawson W.O., 2010. 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 11: 55–67.
Bar-Joseph M., 1978. Cross-protection incompleteness: A possible cause for natural spread of Citrus tristeza virus after a prolonged lag period in Israel. Phytopathology 68: 1110-1111.
Bar-Joseph M., Marcus R., Lee R.F., 1989. The continuous challenge of Citrus tristeza virus control. Annual Review of Phytopathology 27: 291-316.
Bertolini E., Moreno A., Capote N., Olmos A., Vidal A., Pérez J., Cambra M., 2008. Quantitative detection of Citrus tristeza virus in plant tissues and single aphids by real-time RT-PCR. European Journal of Plant Pathology 120: 177-188.
Besoain X., 2008. Incidencia, caracterización y epidemiologia del virus de la tristeza de los cítricos en Chile. Tesis Doctoral, Universidad Politécnica de Valencia, Valencia, España, 129 pp.
Besoain X., Bertolini E., Camps R., Ramella F., Gorris M.T., Torres M. and 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: 251-262.
Blackman R.L. and V.F. Eastop, 2006. Aphids on the World’s herbaceous Plants and Shrubs. An Identification and Information Guide. John Wiley and Sons & The Natural History Museum. Chichester (United Kingdom). 2 vols., 1024 pp.
Brlansky R., Damsteegt V., Howd D. and Roy A., 2003. Molecular analyses of Citrus tristeza virus sub-isolates separated by aphid transmission. Plant Disease 87: 397-40.
Cambra M., Gorris M.T., Marroquín C., Román M., Olmos A., … Navarro L., 2000. Incidence and epidemiology of Citrus tristeza virus in the Valencian Community of Spain. Virus Research 71: 85-95.
Chen A., Watanabe S., Yokomi R. and Ng J.C.K., 2018. Nucleotide heterogeneity at the terminal ends of the genomes of two California Citrus tristeza virus strains and their complete genome sequence analysis. Virology Journal 15: 141.
Dawson W., Bar-Joseph M., Garsney S. and Moreno P., 2015.Citrus tristeza virus making an ally from an enemy. Annual Review of Phytopathology 53: 137-155.
Dawson W., Garnsey S., Tatineni S., Folimonova S., Harper S., Gowda S., 2013. Citrus tristeza virus-host interactions. Frontiers in Microbiology 88: 1-10.
D'urso F., Ayllon M., Rubio L., Sambade A., Hermoso de Mendoza A., Guerri J., Moreno P, 2000. Contribution of uneven distribution of genomic RNA variants of Citrus tristeza virus (CTV) within the plant to changes in the viral population following aphid transmission. Plant Pathology 49: 288-294.
Folimonova S., Robertson C., Shilts T., Folimonov A., Hilf M., Garnsey S., 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.
Fuller S., Chavigny P., Lapchin L., Vanlerberghe-Masutti F., 1999. Variation in clonal diversity in glasshouse infestations of the aphid, Aphis gossypii Glover in southern France. Molecular Ecology 8: 1867-1877.
Garnsey, S.M., Gumpf, D.J., Roistacher, C.N., Civerolo, E.L., Lee, R.F., Yokomi, R.K. and Bar-Joseph, M. 1987. Toward standardized evaluation of the biological properties of citrus tristeza virus. Phytophylactica 19:151-157.
Harper S., 2013. Citrus tristeza virus: evolution of complex and varied genotypic groups. Frontiers in Microbiology 93: 1-18.
Harper S., Dawson T., Pearson M., 2010. Isolates of Citrus tristeza virus that overcome Poncirus trifoliate resistance comprise novel strain. Archives of Virology 155: 471-480.
Harper S., Cowell S., Dawson W.O., 2015. Finding balance: Virus populations reach equilibrium during the infection process. Virology 485: 205–212.
Harper S.J., Cowell S.J., Dawson W.O., 2018. Bottlenecks and complementation in the aphid transmission of Citrus tristeza virus populations. Archives of Virology 163: 3373:3376.
Harper S., Cowell S., Robertson C., Dawson W., 2014. Differential tropism in roots and shoots infected by Citrus tristeza virus. Virology 460: 91-99.
Harper S.J., Killiny N., Tatineni S., Gowda S., Cowell S.J., Shilts T., Dawson W.O, 2016. Sequence variation in two genes determines the efficacy of transmission of Citrus tristeza virus by the brown citrus aphid. Archives of Virology 161: 3555-2559.
Hermoso de Mendoza A., Ballester-Olmos J., Pina J., 1984. Transmission of Citrus tristeza virus by aphids (Homoptera, Aphididae) in Spain. Proceedings of the 9th Conference of International Organization of Citrus Virologists (IOCV). IOCV, Riverside, CA, USA, 23-27.
Hilf M., Mavrodieva A., Garnsey S., 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.
Karasev, A. 2000. Genetic diversity and evolution of Closterovirus. Annual Review Phytopathology 38: 293-324.
Marroquín C., Olmos A., Gorris M.T., Bertolini E., Martínez M.C., … Cambra M., 2004. Estimation of the number of aphids carrying Citrus tristeza virus that visit adult citrus trees. Virus Research 100: 101-108.
Mawassi M., Gafny R., Bar-Joseph M., 1993. Nucleotide sequence of the coat protein gene of Citrus tristeza virus: comparison of biologically diverse isolates collected in Israel. Virus Genes 7: 265–275.
Melzer M.J., Borth W.B., Sether D.M., Ferreira S., Gonsalves D., Hu J., 2010. Genetic diversity and evidence for recent modular recombination in Hawaiian Citrus tristeza virus. Virus Genes 40: 111-118.
Moreno P., Ambros S., Albiach-Martí M., Guerri J., Pena L., 2008. Citrus tristeza virus: a pathogen that changed the course of the citrus industry. Molecular Plant Pathology 9: 251–268.
Nieto J.M., Fuentes-Contreras E., Castro M., Aldea M., Oretego J., Mier M.P., 2016. Catálogo de los áfidos (Hemiptera, Aphididae) de Chile, con plantas hospedadoras y distribuciones regional y provincial. Graellsia 72: 167.
Pappu H., Pappu S., Manjunath K., Lee R., Niblett C., 1993. Molecular characterization of a structural epitope that is largely conserved among severe isolates of a plant virus. Proceedings of the National Academy of Sciences of the USA 90: 3641-3644.
Permar T., Garnsey S., Gumpf D., Lee R., 1990. A monoclonal antibody that discriminates strains of Citrus tristeza virus. Phytopathology 80: 224- 228.
Rocha-Peña M., Lee R., Lastra R., Niblett C., Ochoa-Corona F., Garnsey S., Yokomy R., 1995. Citrus tristeza virus and its aphid vector Toxoptera citricida. Threats of citrus production in the Caribbean and Central and North America. Plant Disease 79: 437-445.
Roy A., Brlansky H., 2009. Population dynamics of a Florida Citrus tristeza virus isolate and aphid-transmitted subisolates: Identification of three genotypic groups and recombinants after aphid transmission. Phytopathology 99: 1297-1306.
Rubio L., Ayllón M.A., Kong P., Fernández A., Polek M., … Falk B.W., 2001. Genetic variation of Citrus tristeza virus isolates from California and Spain: evidence for mixed infections and recombinations. Journal of Virology 75: 8054-8062.
Satyanarayana T., Gowda S., Ayllón M.A., Albiach-Martí M.R., Dawson W.O., 2002. Mutational analysis of the replication signals in the 3′-nontranslated region of Citrus tristeza virus. Virology 300: 140–52.
Schneider W., Roossinck M., 2001. Genetic diversity in RNA virus quasispecies is controlled by host-virus interactions. Journal of Virology 75: 12165-12173.
Scott K., Hlela Q., Zablocki O., Read D., Vuuren S., Pietersen G., 2013. Genotype composition of populations of grapefruit-crossprotecting Citrus tristeza virus strain GFMS12 in different host plants and aphid-transmitted sub-isolates. Archives of Virology 158: 27–37.
Simbaqueba R., Serna F., Posada-Flórez F., 2014. Curaduría, Morfología e identificación de áfidos (Hemiptera: Aphididae) del museo entomológico UNAB. Primera aproximación. Boletín científico museo historia natural. 18:222-246.
Weathers L., Sánchez L., Platt G. 1969. Naturaleza y distribución de las enfermedades virosas de cítricos en Chile. Agricultura Técnica (Chile) 29:166-170.
Yokomi R.K., Selvaraj V., Maheshwari Y., Chiumenti M., Saponari M., ... Hajeri S., 2018. Molecular and biological characterization of a novel mild strain of Citrus tristeza virus in California. Archives of Virology 163: 1795-1804.
Yokomi R.K., DeBorde R.L, 2005. Incidence, transmissibility, and genotype analysis of Citrus tristeza virus (CTV) isolates from CTV eradicative and noneradicative districts in central California. Plant Disease 89: 859-866.