Articles
Published 2021-09-13
Keywords
- Citrus virus,
- vein enation disease,
- woody gall disease,
- CVEV
How to Cite
[1]
M. MINUTOLO, M. CINQUE, G. ALTAMURA, F. DI SERIO, D. ALIOTO, and B. NAVARRO, “Identification, full-length genome sequencing, and field survey of citrus vein enation virus in Italy”, Phytopathol. Mediterr., vol. 60, no. 2, pp. 293–301, Sep. 2021.
Funding data
-
Horizon 2020
Grant numbers No. 734736 -
Regione Campania
Grant numbers URCOFI (DGR 690/2016, 6th December 2016 -
Regione Puglia
Grant numbers INNOCI DGR n. 903/ 2012 15th May 2012
Abstract
Citrus vein enation virus (CVEV) was described in Spain and then it has been reported in several citrus growing areas of Asia, America and Australia. Here, the occurrence of CVEV in Italy has been documented for the first time. The full genome sequence of a CVEV Italian isolate (14Q) was determined by high-throughput sequencing and the presence of the virus was confirmed by RT-PCR and graft-transmission to indicator plants, from which the virus was recovered six-months post-inoculation. Phylogenetic analysis based on the full-length genome of CVEV isolates from different countries showed that they are phylogenetically related to each other based on their geographic origin, rather than on their host and that the Italian isolate is more closely related to the Spanish isolate than to the other ones. A field survey revealed the presence of CVEV in some areas of Campania region (southern Italy), prevalently infecting lemon trees. In the frame of this survey, kumquat was identified for the first time as a host of CVEV. No symptoms were observed in the field so far. The infection of asymptomatic hosts and the transmission by aphid species present in Italy increase the risk that the virus could further spread.
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References
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Bankevich A., Nurk S., Antipov D., Gurevich A.A., Dvorkin M., … Pevzner P.A., 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology 19: 455-477. https://doi.org/10.1089/cmb.2012.0021.
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Chabi-Jesus C., Ramos-González P.L., Tassi A.D., Guerra-Peraza O., Kitajima E.W., … Freitas-Astúa J., 2018. Identification and Characterization of Citrus Chlorotic Spot Virus, a New Dichorhavirus Associated with Citrus Leprosis-Like Symptoms. Plant Disease 102: 1588-1598. https://doi.org/10.1094/PDIS-09-17-1425-RE.
Chabi-Jesus C., Najar A., Fontenele R.S., Kumari S.G., Ramos-González P.L., … Varsani A., 2020. Viruses representing two new genomovirus species identified in citrus from Tunisia. Archives in Virology 165: 1225-1229. https://asu.pure.elsevier.com/en/publications/viruses-representing-two-new-genomovirus-species-identified-in-ci.
Chen G.Q., Yan S.X., Roistacher C.N., 1992. First report of citrus vein enation disease in China. Plant Disease 76: 1077. https://www.apsnet.org/publications/plantdisease/backissues/Documents/1992Abstracts/PD_76_1077C.htm
Fraser L. R., 1959. Woody gall, a suspected virus disease of rough lemon and other citrus varieties. Proceedings of the Linnean Society of New South Wales 84: 332-336.
Harakava R., Salaroli R.B., Freitas-Astúa J., 2017. Citrus leprosis virus N: A New Dichorhavirus Causing Citrus Leprosis Disease. Phytopathology 107: 963-976. https://doi.org/10.1094/PHYTO-02-17-0042-R
Hermoso de Mendoza A., Pina J.A., Ballester-Olmos J.F., Navarro L., 1993. Persistent transmission of Citrus vein enation virus by Aphis gossypii and Myzus persicae. In: Proc. 12th Conf. Intern. Organization Citrus Virol. (P. Moreno, J. V. da Graça, and L. W. Timmer, ed.), IOCV, Riverside, CA, USA, 361-362
Huang A., Song Z., Cao M., Chen H., Li Z., Zhou C., 2015. The complete genome sequence of Citrus vein enation virus from China. Journal of Integrative Agriculture 14: 598–601. https://doi.org/10.1016/S2095-3119(14)60903-5
Langmead B., Trapnell C., Pop M., Salzberg S.L., 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10: R25. https://genomebiology.biomedcentral.com/articles/10.1186/gb-2009-10-3-r25
Loconsole G., Onelge N., Potere O., Giampetruzzi A., Bozan O., … Saponari M., 2012a. Identification and characterization of citrus yellow vein clearing virus, a putative new member of the genus Mandarivirus. Phytopathology 102: 1168-175. https://apsjournals.apsnet.org/doi/pdf/10.1094/PHYTO-06-12-0140-R
Loconsole G., Saldarelli P., Doddapaneni H., Savino V., Martelli G.P., Saponari M., 2012b. Identification of a single-stranded DNA virus associated with citrus chlorotic dwarf disease, a new member in the family Geminiviridae. Virology 432: 162-172. https://doi.org/10.1016/j.virol.2012.06.005
Maliogka V.I., Minafra A., Saldarelli P., Ruiz-García A.B., Glasa M., ... Olmos A., 2018 Recent Advances on Detection and Characterization of Fruit Tree Viruses Using High-Throughput Sequencing Technologies. Viruses 10: 436. d https://doi.org/10.3390/v10080436
Maharaj S.B., da Graça J.V., 1989. Transmission of citrus vein enation virus by Toxoptera citricidus. Phytophylactica 21: 81-82.
Moreno P., 2000. Protuberancias nerviales-Agallas de la madera (Vein enation-Woody gall). In: Enfermedades de los cítricos. Monografía de la Sociedad Española de Fitopatología no. 2 (N. Duran- Vila and P. Moreno, ed.), Ediciones Mundi-Prensa, Madrid, Spain. 74-75
Nakazono-Nagaoka E., Fujikawa T., Iwanami T., 2017. Nucleotide sequences of Japanese isolates of citrus vein enation virus. Archives in Virology 62: 879-883. doi: 10.1007/s00705-016-3139-6. https://link.springer.com/article/10.1007/s00705-016-3139-6
Navarro B., Loconsole G., Giampetruzzi A., Aboughanem-Sabanadzovic N., Ragozzino A., … Di serio F., 2017. Identification and characterization of privet leaf blotch-associated virus, a novel idaeovirus. Molecular Plant Pathology 18: 925-936. https://doi.org/10.1111/mpp.12450
Navarro B., Minutolo M., De Stradis A., Palmisano F., Alioto D., Di Serio F., 2018a. The first phlebo-like virus infecting plants: a case study on the adaptation of negative-stranded RNA viruses to new hosts. Molecular Plant Pathology 19: 1075-1089. https://doi.org/10.1111/mpp.12587
Navarro B., Zicca S., Minutolo M., Saponari M., Alioto D., Di Serio F., 2018b. A Negative-Stranded RNA Virus Infecting Citrus Trees: The Second Member of a New Genus Within the Order Bunyavirales. Frontiers in Microbiology 9: 2340. https://doi.org/10.3389/fmicb.2018.02340.
Pallás V., Navarro A., Flores R.,1987. Isolation of a viroid-like RNA from hop different from hop stunt viroid. Journal of General Virology 68: 2095–2102.
Ramos-González P.L., Chabi-Jesus C., Guerra-Peraza O., Tassi A.D., Kitajima EW, … Freitas-Astúa J., 2017. Citrus leprosis virus N: A New Dichorhavirus Causing Citrus Leprosis Disease. Phytopathology 107: 963-976. https://doi.org/10.1094/PHYTO-02-17-0042-R
Roy A., Choudhary N., Guillermo L.M., Shao J., Govindarajulu A., … Brlansky R.H., 2013. A novel virus of the genus Cilevirus causing symptoms similar to citrus leprosis. Phytopathology 103: 488-500. https://apsjournals.apsnet.org/doi/pdf/10.1094/PHYTO-07-12-0177-R
Sievers F., Higgins D.G., 2014. Clustal Omega, accurate alignment of very large numbers of sequences. Methods in Molecular Biology 1079: 105-116. https://link.springer.com/protocol/10.1007/978-1-62703-646-7_6
Vives M.C., Velázquez K., Pina J.A., Moreno P., Guerri J., Navarro L., 2013. Identification of a new enamovirus associated with citrus vein enation disease by deep sequencing of small RNAs. Phytopathology 103: 1077-1086. https://doi.org/10.1094/PHYTO-03-13-0068-R
Wallace J.M., Drake R., 1953. A virus-induced vein enation in citrus. Citrus Leaves 33: 22–24.
Wallace J.M., Drake R.J., 1960. Woody galls on citrus associated with vein-enation virus infection. Plant Disease Reporter 44: 580-584.
Wu J., Liu Q., Qiu Y., Zhang S., Li Z., … Cao M., 2019. First Report of Citrus Vein Enation Virus from Citrus Cultivar Huangguogan in Sichuan Province, China. Plant Disease 103. https://apsjournals.apsnet.org/doi/10.1094/PDIS-03-19-0461-PDN
Wu J., Zhang S., Atta S., Yang C., Zhou Y., … Cao M., 2020. Discovery and Survey of a New Mandarivirus Associated with Leaf Yellow Mottle Disease of Citrus in Pakistan. Plant Disease 104: 1593-1600. https://doi.org/10.1094/PDIS-08-19-1744-RE
Xuan Z., Li S., Zhang S., Ran W., Zhou Y., … Cao M., 2020. Complete genome sequence of citrus yellow spot virus, a newly discovered member of the family Betaflexiviridae. Archives in Virology 165: 2709–2713. https://link.springer.com/article/10.1007/s00705-020-04794-1
Yang H.J., Oh J., Lee H.K., Lee D. S., Kim S.Y., … Lee S.H., 2019. First Report of Citrus Vein Enation Virus in Satsuma Mandarin (Citrus unshiu) in Korea. Plant Disease 103: 2703. https://doi.org/10.1094/PDIS-03-19-0468-PDN
Bankevich A., Nurk S., Antipov D., Gurevich A.A., Dvorkin M., … Pevzner P.A., 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology 19: 455-477. https://doi.org/10.1089/cmb.2012.0021.
Catara A., Davino M., 1984. Citrus diseases not found in Italy, caused by viruses and virus-like pathogens. Informatore Fitopatologico 34: 9-21.
Chabi-Jesus C., Ramos-González P.L., Tassi A.D., Guerra-Peraza O., Kitajima E.W., … Freitas-Astúa J., 2018. Identification and Characterization of Citrus Chlorotic Spot Virus, a New Dichorhavirus Associated with Citrus Leprosis-Like Symptoms. Plant Disease 102: 1588-1598. https://doi.org/10.1094/PDIS-09-17-1425-RE.
Chabi-Jesus C., Najar A., Fontenele R.S., Kumari S.G., Ramos-González P.L., … Varsani A., 2020. Viruses representing two new genomovirus species identified in citrus from Tunisia. Archives in Virology 165: 1225-1229. https://asu.pure.elsevier.com/en/publications/viruses-representing-two-new-genomovirus-species-identified-in-ci.
Chen G.Q., Yan S.X., Roistacher C.N., 1992. First report of citrus vein enation disease in China. Plant Disease 76: 1077. https://www.apsnet.org/publications/plantdisease/backissues/Documents/1992Abstracts/PD_76_1077C.htm
Fraser L. R., 1959. Woody gall, a suspected virus disease of rough lemon and other citrus varieties. Proceedings of the Linnean Society of New South Wales 84: 332-336.
Harakava R., Salaroli R.B., Freitas-Astúa J., 2017. Citrus leprosis virus N: A New Dichorhavirus Causing Citrus Leprosis Disease. Phytopathology 107: 963-976. https://doi.org/10.1094/PHYTO-02-17-0042-R
Hermoso de Mendoza A., Pina J.A., Ballester-Olmos J.F., Navarro L., 1993. Persistent transmission of Citrus vein enation virus by Aphis gossypii and Myzus persicae. In: Proc. 12th Conf. Intern. Organization Citrus Virol. (P. Moreno, J. V. da Graça, and L. W. Timmer, ed.), IOCV, Riverside, CA, USA, 361-362
Huang A., Song Z., Cao M., Chen H., Li Z., Zhou C., 2015. The complete genome sequence of Citrus vein enation virus from China. Journal of Integrative Agriculture 14: 598–601. https://doi.org/10.1016/S2095-3119(14)60903-5
Langmead B., Trapnell C., Pop M., Salzberg S.L., 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10: R25. https://genomebiology.biomedcentral.com/articles/10.1186/gb-2009-10-3-r25
Loconsole G., Onelge N., Potere O., Giampetruzzi A., Bozan O., … Saponari M., 2012a. Identification and characterization of citrus yellow vein clearing virus, a putative new member of the genus Mandarivirus. Phytopathology 102: 1168-175. https://apsjournals.apsnet.org/doi/pdf/10.1094/PHYTO-06-12-0140-R
Loconsole G., Saldarelli P., Doddapaneni H., Savino V., Martelli G.P., Saponari M., 2012b. Identification of a single-stranded DNA virus associated with citrus chlorotic dwarf disease, a new member in the family Geminiviridae. Virology 432: 162-172. https://doi.org/10.1016/j.virol.2012.06.005
Maliogka V.I., Minafra A., Saldarelli P., Ruiz-García A.B., Glasa M., ... Olmos A., 2018 Recent Advances on Detection and Characterization of Fruit Tree Viruses Using High-Throughput Sequencing Technologies. Viruses 10: 436. d https://doi.org/10.3390/v10080436
Maharaj S.B., da Graça J.V., 1989. Transmission of citrus vein enation virus by Toxoptera citricidus. Phytophylactica 21: 81-82.
Moreno P., 2000. Protuberancias nerviales-Agallas de la madera (Vein enation-Woody gall). In: Enfermedades de los cítricos. Monografía de la Sociedad Española de Fitopatología no. 2 (N. Duran- Vila and P. Moreno, ed.), Ediciones Mundi-Prensa, Madrid, Spain. 74-75
Nakazono-Nagaoka E., Fujikawa T., Iwanami T., 2017. Nucleotide sequences of Japanese isolates of citrus vein enation virus. Archives in Virology 62: 879-883. doi: 10.1007/s00705-016-3139-6. https://link.springer.com/article/10.1007/s00705-016-3139-6
Navarro B., Loconsole G., Giampetruzzi A., Aboughanem-Sabanadzovic N., Ragozzino A., … Di serio F., 2017. Identification and characterization of privet leaf blotch-associated virus, a novel idaeovirus. Molecular Plant Pathology 18: 925-936. https://doi.org/10.1111/mpp.12450
Navarro B., Minutolo M., De Stradis A., Palmisano F., Alioto D., Di Serio F., 2018a. The first phlebo-like virus infecting plants: a case study on the adaptation of negative-stranded RNA viruses to new hosts. Molecular Plant Pathology 19: 1075-1089. https://doi.org/10.1111/mpp.12587
Navarro B., Zicca S., Minutolo M., Saponari M., Alioto D., Di Serio F., 2018b. A Negative-Stranded RNA Virus Infecting Citrus Trees: The Second Member of a New Genus Within the Order Bunyavirales. Frontiers in Microbiology 9: 2340. https://doi.org/10.3389/fmicb.2018.02340.
Pallás V., Navarro A., Flores R.,1987. Isolation of a viroid-like RNA from hop different from hop stunt viroid. Journal of General Virology 68: 2095–2102.
Ramos-González P.L., Chabi-Jesus C., Guerra-Peraza O., Tassi A.D., Kitajima EW, … Freitas-Astúa J., 2017. Citrus leprosis virus N: A New Dichorhavirus Causing Citrus Leprosis Disease. Phytopathology 107: 963-976. https://doi.org/10.1094/PHYTO-02-17-0042-R
Roy A., Choudhary N., Guillermo L.M., Shao J., Govindarajulu A., … Brlansky R.H., 2013. A novel virus of the genus Cilevirus causing symptoms similar to citrus leprosis. Phytopathology 103: 488-500. https://apsjournals.apsnet.org/doi/pdf/10.1094/PHYTO-07-12-0177-R
Sievers F., Higgins D.G., 2014. Clustal Omega, accurate alignment of very large numbers of sequences. Methods in Molecular Biology 1079: 105-116. https://link.springer.com/protocol/10.1007/978-1-62703-646-7_6
Vives M.C., Velázquez K., Pina J.A., Moreno P., Guerri J., Navarro L., 2013. Identification of a new enamovirus associated with citrus vein enation disease by deep sequencing of small RNAs. Phytopathology 103: 1077-1086. https://doi.org/10.1094/PHYTO-03-13-0068-R
Wallace J.M., Drake R., 1953. A virus-induced vein enation in citrus. Citrus Leaves 33: 22–24.
Wallace J.M., Drake R.J., 1960. Woody galls on citrus associated with vein-enation virus infection. Plant Disease Reporter 44: 580-584.
Wu J., Liu Q., Qiu Y., Zhang S., Li Z., … Cao M., 2019. First Report of Citrus Vein Enation Virus from Citrus Cultivar Huangguogan in Sichuan Province, China. Plant Disease 103. https://apsjournals.apsnet.org/doi/10.1094/PDIS-03-19-0461-PDN
Wu J., Zhang S., Atta S., Yang C., Zhou Y., … Cao M., 2020. Discovery and Survey of a New Mandarivirus Associated with Leaf Yellow Mottle Disease of Citrus in Pakistan. Plant Disease 104: 1593-1600. https://doi.org/10.1094/PDIS-08-19-1744-RE
Xuan Z., Li S., Zhang S., Ran W., Zhou Y., … Cao M., 2020. Complete genome sequence of citrus yellow spot virus, a newly discovered member of the family Betaflexiviridae. Archives in Virology 165: 2709–2713. https://link.springer.com/article/10.1007/s00705-020-04794-1
Yang H.J., Oh J., Lee H.K., Lee D. S., Kim S.Y., … Lee S.H., 2019. First Report of Citrus Vein Enation Virus in Satsuma Mandarin (Citrus unshiu) in Korea. Plant Disease 103: 2703. https://doi.org/10.1094/PDIS-03-19-0468-PDN