Severe <i>Citrus tristeza virus</i> Isolates from Eastern Mexico Are Related to the T36 Genotype Group — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Severe <i>Citrus tristeza virus</i> Isolates from Eastern Mexico Are Related to the T36 Genotype Group
Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias-Campo Experimental Valle de México, Carretera Los Reyes-Texcoco km 13.5, Coatlinchán, Texcoco, México
,
Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias-Campo Experimental Ixtacuaco, Carretera Martínez de la Tor-re-Tlapacoyan km 4.5, Tlapacoyan, Veracruz, México
,
Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias-Campo Experimental Ixtacuaco, Carretera Martínez de la Tor-re-Tlapacoyan km 4.5, Tlapacoyan, Veracruz, México
,
Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias-Campo Experimental Mocochá, Carretera Mérida-Motul km 25, Mocochá, Yucatán, México
,
School of Agricultural Sciences, Northwest Missouri State University, Maryville, USA
,
Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias-Campo Experimental Ixtacuaco, Carretera Martínez de la Torre-Tlapacoyan km 4.5, Tlapacoyan, Veracruz, México
,
Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias-Campo Experimental Mocochá, Carretera Mérida-Motul km 25, Mocochá, Yucatán, México
1 Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias-Campo Experimental Valle de México, Carretera Los Reyes-Texcoco km 13.5, Coatlinchán, Texcoco, México
2 Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias-Campo Experimental Ixtacuaco, Carretera Martínez de la Tor-re-Tlapacoyan km 4.5, Tlapacoyan, Veracruz, México
3 Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias-Campo Experimental Ixtacuaco, Carretera Martínez de la Tor-re-Tlapacoyan km 4.5, Tlapacoyan, Veracruz, México
4 Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias-Campo Experimental Mocochá, Carretera Mérida-Motul km 25, Mocochá, Yucatán, México
5 School of Agricultural Sciences, Northwest Missouri State University, Maryville, USA
6 Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias-Campo Experimental Ixtacuaco, Carretera Martínez de la Torre-Tlapacoyan km 4.5, Tlapacoyan, Veracruz, México
7 Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias-Campo Experimental Mocochá, Carretera Mérida-Motul km 25, Mocochá, Yucatán, México
Citrus tristeza virus (CTV) outbreaks have been reported in the main citrus growing region of Mexico in the past four years. Recently, in eastern Mexico (the major citrus-growing region in the country), severe CTV isolates have been detected. However, the molecular identity of observed isolates remains unestablished. This research was undertaken to elucidate the molecular characterization of CTV populations spreading in this region and to compare it with phylogeny of existing isolates. Genotyping of 32 collected isolates was performed using reverse-transcription polymerase chain reaction (RT-PCR) with sequence analysis of the coat protein (CP) gene, putatively associated with pathogenicity. This protein is a 25 kDa major capsid protein, which forms a long virion body coating 95% of the particle length. A comparative sequence analys is was performed using CTV sequences from different geographical origins already published and deposited in the GenBank databases. Phylogenetic analysis showed that the degree of sequence divergence among isolates correlated with their pathogenicity. Based on the sequencing results, the collected isolates were categorizedn as mild or severe phylogenetic clusters, each being genetically distinct. The severe group was associated with either a - like or with a T36-like genotype. The latter group matched with the quick decline and stem pitting drastic symptoms observed in the field. This study identified the presence of severe CTV isolates related to the T36-like genotype and to the cause of quick decline and stem pitting in sweet orange propagated on sour orange rootstock. Knowledge derived from these analyses could serve to design management strategies for this disease and to understand the cur rent epidemic outbreak in scenarios where the most efficient vector is present.
KeywordsCTVEpidemiologySevere IsolatesStem PittingQuick DeclineCoat Protein Gene
Bar-Joseph, M., Batuman, O. and Roistacher, C.N. (2010) The History of Citrus tristeza virus—Revisited. In: Karasev, A.V. and Hilf, M.E., Eds., Citrus tristeza virus Complex and Tristeza Diseases, APS Press, St. Paul, 3-26.
Moreno, P., Ambros, S., Albiachi-Marti, M.R., Guerri, J. and Pena, L. (2008) Citrus tristeza vírus: A Pathogen That Changed the Course of the Citrus Industry. Molecular Plant Pathology, 9, 251-268. https://doi.org/10.1111/j.1364-3703.2007.00455.x
SIAP (2019) Servicio de Información Agroalimentaria y Pesquera. Consultado online el 10 de abril de 2020. http://infosiap.siap.gob.mx:8080/agricola_siap_gobmx/AvanceNacionalSinPrograma.do
Gottwald, T.R., Garnsey, S.M., Cambra, M., Moreno, P., Irey, M. and Borbon, J. (1997) Comparative Effects of Aphid Vector Species on Increase and Spread of Citrus tristeza virus. Fruits, 52, 397-404.
Loeza-Kuk, E., Ochoa-Martínez, D., Mora-Aguilera, G., Rivas-Valencia, P., Gutiérrez-Espinosa A., Cintra de Jesús Junior, W., Villegas-Monter, A. and Arno Wulff, N. (2008) Acquisition of CSDAV and Haplotypes of Citrus tristeza virus by Toxopetera citricida and Aphis spiraecola and the Implication on Citrus Sudden Death. Agrociencia, 42, 669-678.
Hermoso de Mendoza, A., Ballester-Olmos, J.F. and Pina, L.J.A. (1984) Transmission of Citrus tristeza virus by Aphids (Homoptera, Aphididae) in Spain. International Organization of Citrus Virologists Conference Proceedings (1957-2010), 9, 23-27. https://escholarship.org/uc/item/5zj9877d
Raccah, H.B., Loebenstein, G. and Singer, S. (1980) Aphid Transmissibility Variants of Citrus tristeza virus in Infected Citrus Trees. Phytopathology, 70, 89-93. https://doi.org/10.1094/Phyto-70-89
López-Arroyo, J.I., Loera-Gallardo, J., Rocha-Pena, M.A., Canales, R., Hernández, I., Reyes, M.A., Berlanga, A. and Miranda, M.A. (2008) Pulgón café de los cítricos, Toxoptera citricida (Hemíptera: Aphididdae). In: Arredondo, H.C. and Rodríguez, L.A., Eds., Casos de control biológico en México, Grupo Mundi-Prensa, México, 279-292.
Febres, V.J., Ashoulin, L., Mawassi, M., Frank, A., Bar-Joseph, M., Manjunath, K.L., Lee, R.F. and Niblett, C.L. (1996) The p27 Protein Is Present at One End of Citrus tristeza virus Particles. Phytopathology, 86, 1331-1335.
Satyanarayana, T., Gowda, S., Ayllón, M.A. and 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. Proceedings of the National Academy of Sciences of the United States of America, 101, 799-804. https://doi.org/10.1073/pnas.0307747100
Moreno, P., Guerri, J., Ballester-Olmos, J.F., Albiach, R. and 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 Pathology, 42, 35-41. https://doi.org/10.1111/j.1365-3059.1993.tb01469.x
Powell, C.A., Pelosi, R.R. and Cohen, M. (1992) Superinfection of Orange Trees Containing Mild Isolates of Citrus tristeza virus with Severe Florida Isolates of Citrus tristeza virus. Plant Disease, 76, 141-144. https://doi.org/10.1094/PD-76-0141
Roistacher, C.N. and Moreno, P. (1991) The Worldwide Threat from Destructive Isolates of Citrus tristeza virus a Review. Proceedings 11th Conference International Organization of Citrus Virologists, IOCV, Riverside, 7-19.
Harper, S.J. (2013) Citrus tristeza virus: Evolution of Complex and Varied Genotypic Groups. Frontiers in Microbiology, 4, 93. https://doi.org/10.3389/fmicb.2013.00093
Herrera-Isidrón, L., Ochoa-Sánchez, J.C., Rivera-Bustamante, R. and Martínez-Soriano, J.P. (2009) Sequence Diversity on Four ORFs of Citrus tristeza virus Correlates with Pathogenicity. Virology Journal, 6, Article No. 116. https://doi.org/10.1186/1743-422X-6-116
Rivas-Valencia, P., Loeza-Kuk, E., Domínguez-Monge, S. and Lomas-Barrié, C.T. (2017) Chronic Infection of the Citrus tristeza virus in Citrus sinensis/C. aurantium Trees in a Restrictive Thermal Regime in Yucatán. Revista Chapingo Serie Horticultura, 23, 187-202. https://doi.org/10.5154/r.rchsh.2016.11.028
Domínguez-Monge, S., Mora-Aguilera, G., Loeza-Kuk, E., Gutiérrez-Espinosa, M.A., Flores-Sánchez, J., Acevedo-Sánchez, G., Ochoa-Martinez, D., Febres, V., Hernández-Nava, G. and Martínez-Bustamante, V. (2014) Epidemiología molecular de aislamientos de citrus tristeza virus de la Península de Yucatán. Revista Mexicana de Fitopatología, 32, 46.
Domínguez-Monge, S., Mora-Aguilera, G., Loeza-Kuk, E., Rivas-Valencia, P., Ruiz-García, N., Días-Padilla, G., Acevedo-Sánchez, G., Munguía-Rosales, R., Velázquez-Toledo, J., Escalante-Márquez, F. and Robles-García, P. (2010) Regionalización epidemiológica de la tristeza de los cítricos en la Península de Yucatán. V Reunión Nacional de Innovación Agrícola, Campeche, 22-27 noviembre 2010, 334.
Rivas, V.P., Loeza, K.E., Mora-Aguilera, G., Ruiz, G.N., Ochoa, M.D., Gutiérrez, E.A. and Febres, V. (2010) Análisis Espacio-Temporal de aislamientos del Citrus tristeza virus de Yucatán y Tamaulipas. Revista Mexicana de Ciencias Agrícolas, 1, 493-507.
Loeza-Kuk, E., Palacios-Torres, E.C., Ochoa-Martínez, D., Mora-Aguilera, G., Gutiérrez-Espinosa, M.A., Febres, V.J., Moore, G.A. and Alvarez-Ramos, R. (2005) Molecular Characterization of Citrus tristeza virus Isolates from Veracruz and Tamaulipas States, México. In: Hilf, M.E., Duran-Vila, A. and Rocha-Pena, M.A., Eds., Proceedings 16th IOCV Conference, International Organization of Citrus Virologists and University of California, Riverside, CA, USA, 407-411. https://www.researchgate.net/publication/267417106_Molecular_Characterization_ of_Citrus_tristeza_virus_Isolates_from_Veracruz_and_Tamaulipas_States_Mexico
López-Vera, E.E., Domínguez-Monge, S., Santillán-Mendoza, R., Rodríguez-Quibrera, C. and Martínez-Rivera, N. (2019) Ocurrencia de aislamientos severos del Citrus tristeza virus en árboles de naranja dulce en Veracruz. XXXII Reunión Científica-Tecnológica, Forestal y Agropecuaria y IV Congreso Mexicano de Investigación en Cítricos, World Trade Center, Boca del Río, Veracruz, 14 y 15 de Noviembre, 529-534.
Harris, A. (2002) Nepoviruses and Their Diagnosis in Plants: A Novel Polymerase Chain Reaction Diagnostic Test for Nepoviruses in Nursery Stock. Biosecurity Australia, Biosecurity Australia
Bonfield, J.K. and Whitwham, A. (2010) Gap5—Editing the Billion Fragment Sequence Assembly. Bioinformatics. 26, 1699-1703. https://doi.org/10.1093/bioinformatics/btq268
Edgar, R.C. (2004) MUSCLE: Multiple Sequence Alignment with High Accuracy and High Throughput. Nucleic Acids Research, 32, 1792-1797. https://doi.org/10.1093/nar/gkh340
Swofford, D.L. (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.0 a 167. Sinauer Associates, Sunderland, MA.
Ronquist, F., Teslenko, M., Van der Mark P., Ayres, D.L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M.A. and Huelsenbeck, J.P. (2012) MrBayes 3.2: Efficient Bayesian phylogenetic Inference and Model Choice across a Large Model Space. Systematic Biology, 61, 539-542. https://doi.org/10.1093/sysbio/sys029
Maddison, W.P. and Maddison, D.R. (2019) Mesquite: A Modular System for Evolutionary Analysis. Version 3.61. http://mesquiteproject.org
Albiach-Marti, M.R., Mawassi, M., Gowda, S., Satyanarayana, T., Hilf, M.E., Shanker, S., Almira, E.C., Vives, M.C., Lopez, C., Guerri, J., Flores, R., Moreno, P., Garnsey, S.M. and Dawson, W.O. (2000) Sequences of Citrus tristeza virus Separated in Time and Space Are Essentially Identical. Journal of Virology, 74, 6856-6865. https://doi.org/10.1128/JVI.74.15.6856-6865.2000
Mawassi, M., Mietkiewska, E., Gofman, R., Yang, G. and Bar-Joseph, M. (1996) Unusual Sequence Relationships between Two Isolates of Citrus tristeza virus. Journal of General Virology, 77, 2359-2364. https://doi.org/10.1099/0022-1317-77-9-2359
Vives, M.C., Rubio, L., Lopez, C., Navas-Castillo, J., Albiach-Marti, M.R., Dawson, W.O., Guerri, J., Flores, R. and Moreno, P. (1999) The Complete Genome Sequence of the Major Component of a Mild Citrus tristeza virus Isolate. Journal of General Virology, 80, 811-816. https://doi.org/10.1099/0022-1317-80-3-811
Yang, Z.N., Mathews, D.M., Dodds, J.A. and Mirkov, T.E. (1999) Molecular Characterization of an Isolate of Citrus tristeza virus That Causes Severe Symptoms in Sweet Orange. Virus Genes, 19, 131-142. https://doi.org/10.1023/A:1008127224147
Suastika, G., Natsuaki, T., Terui, H., Kano, T.H.I. and Okuda, S. (2001) Nucleotide Sequence of Citrus tristeza virus Seedling Yellows Isolates. Journal of General Plant Pathology, 67, 73-77. https://doi.org/10.1007/PL00012992
Quiroz, V.J.C., Pena del Rio, M.A., Cruz, H.A., Fernández, D.S., González, P.M. and Mendoza, H.A. (2008) Secuencia del genoma de un aislamiento del virus de la tristeza de los cítricos. Revista Fitotecnia Mexicana, 31, 95-104.
Harper, S.J., Dawson, T.E. and Pearson, M.N. (2009) Complete Genome Sequences of Two Distinct and Diverse Citrus tristeza virus Isolates from New Zealand. Archives of Virology, 154, 1505-1510. https://doi.org/10.1007/s00705-009-0456-z
Domínguez-Monge, S., Mora-Aguilera, G., Loeza-Kuk, E., Flores-Sánchez, J., Acevedo-Sánchez, G. and Robles-García, P. (2012) Implication of Toxoptera citricida on Temporal and Spatial Dispersion the Citrus tristeza virus in Southern Mexico. 12th International Citrus Congress, 18th-23rd November 2012, 240.
Broadbent, P., Brlansky, R.H. and Indsto, J. (1996) Biological Characterization of Australian Isolates of Citrus tristeza virus and Separation of Subisolates by Single Aphid Transmissions. Plant Disease, 80, 329-333. https://doi.org/10.1094/PD-80-0329
Ballester-Olmos, J.F., Pina, J.A., Carbonell, E.A., Moreno, P., Hermoso de Mendoza, A., Cambra, M. and Navarro, L. (1993) Biological Diversity of Citrus tristeza virus (CTV) Isolates in Spain. Plant Pathology, 42, 219-229. https://doi.org/10.1111/j.1365-3059.1993.tb01494.x
Yokomi, R., Lastra, R., Stoetzel, M.B., Damsteegt, V.D., Lee, R.F., Garnsey, S.M., Gottwald, T.R., Rocha-Pena, M.A. and Niblett, C.L. (1994) Establishment of the Brown Citrus Aphid (Homoptera: Aphididae) in Central America and the Caribbean basin and Transmission of Citrus tristeza virus. Journal of Economic Entomology, 87, 1078-1085. https://doi.org/10.1093/jee/87.4.1078
Rivas-Valencia, P., Loeza-Kuk, E., Domínguez-Monge, S. and Mora-Aguilera, G. (2015) Prevalencia de aislamientos tipo T-30 del Citrus Tristeza Virus (CTV) en Yucatán, México. Revista Mexicana de Fitopatología, 33, 230.
Pappu, H., Pappu, S., Niblett, C., Lee, R. and Civerolo, E. (1993) nComparative Sequence Analysis of the Coat Proteins of Biologically Distinct Citrus tristeza closterovirus Isolates. Virus Genes, 7, 255-264. https://doi.org/10.1007/BF01702586
Sambade, A., Lopez, C., Rubio, L., Flores, R., Guerri, J. and 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. https://doi.org/10.1007/s00705-003-0191-9
SENASICA (2020) Plagas Reglamentadas de los Cítricos. Virus de la tristeza de los cítricos—Severo. Servicio Nacional de Sanidad, Inocuidad y Calidad Agroalimentaria-Dirección General de Sanidad Vegetal. http://sinavef.senasica.gob.mx/MDF/