Minor Variants of Orf1a, p33, and p23 Genes of VT Strain Citrus Tristeza Virus Isolates Show Symptomless Reactions on Sour Orange and Prevent Superinfection of Severe VT Isolates
Abstract
:1. Introduction
2. Materials and Methods
2.1. Selection of Source Plants
2.2. Selection of No-SY Isolates
2.3. Molecular Assessment of Genotype
2.4. Biological Stability of Protective Isolates Mac39 and Mac101 in Different Hosts
2.5. Long-Term Assays on Sour Orange and Sweet Orange on SO and Alemow
2.6. Short-Term Tests of Cross-Protection Trials
2.7. High-Throughput Genome Sequencing
2.8. Sequencing of p33 and p23 PCR Amplicons
2.9. Bioinformatics Analysis
3. Results
3.1. Selection of No-SY Source Tree Isolates Spreading in Different Areas of Sicily
3.2. Long-Term Trials Show No-SY VT Isolates Induce Durable Cross-Protection
3.3. Short-Term Trials Confirm Cross-Protection in Different Combinations
3.4. Genome Analysis Reveals No-SY Isolates Are Nucleotide Variants of the SY SG29 Isolate
3.5. The Nucleotide Variations on the p33 and p23 Genes Are Conserved in All the No-SY Isolates
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Martelli, G.P.; Abou Ghanem-Sabanadzovic, N.; Agranovsky, A.A.; Al Rwahnih, M.; Dolja, V.V.; Dovas, C.; Fuchs, M.; Gugerli, P.; Hu, J.S.; Jelkmann, W.; et al. Taxonomic revision of the family Closteroviridae with special reference to grapevine leafroll-associated members of the genus Ampelovirus and the putative species unassigned to the family. J. Plant Pathol. 2012, 94, 7–19. [Google Scholar]
- Karasev, A.V.; Boyko, V.P.; Gowda, S.; Nikolaeva, O.V.; Hilf, M.E.; Koonin, E.V.; Niblett, C.L.; Cline, K.; Gumpf, D.J.; Lee, R.F.; et al. Complete sequence of the Citrus tristeza virus RNA genome. Virology 1995, 208, 511–520. [Google Scholar] [CrossRef]
- Fraser, L. Seedling yellows, an unreported virus disease of citrus. Agric. Gaz. N.S.W. 1952, 63, 125–131. [Google Scholar]
- Bar-Joseph, M.; Marcus, R.; Lee, R.F. The continuous challenge of citrus tristeza virus control. Annu. Rev. Phytopathol. 1989, 27, 291–316. [Google Scholar] [CrossRef]
- Dawson, W.O.; Robertson, C.J.; Albiach-Martí, M.R.; Bar-Joseph, M.; Garnsey, S.M. Mapping sequences involved in induction of decline by citrus tristeza virus T36 on the sour orange rootstock. J. Citrus Pathol. 2015, 2. [Google Scholar] [CrossRef]
- Moreno, P.; Ambrós, S.; Albiach-Martí, M.R.; Guerri, J.; Peña, L. Citrus tristeza virus: A pathogen that changed the course of the citrus industry. Mol. Plant Pathol. 2008, 9, 251–268. [Google Scholar] [CrossRef]
- Fu, S.; Shao, J.; Zhou, C.; Hartung, J.S. Co-infection of sweet orange with severe and mild strains of Citrus tristeza virus is overwhelmingly dominated by the severe strain on both the transcriptional and biological levels. Front. Plant Sci. 2017, 8, 1419. [Google Scholar] [CrossRef] [PubMed]
- Davino, S.; Willemsen, A.; Panno, S.; Davino, M.; Catara, A.; Elena, S.F.; Rubio, L. Emergence and phylodynamics of citrus tristeza virus in Sicily, Italy. PLoS ONE 2013, 8, e66700. [Google Scholar] [CrossRef]
- Licciardello, G.; Raspagliesi, D.; Bar-Joseph, M.; Catara, A. Characterization of isolates of citrus tristeza virus by sequential analyses of enzyme immunoassays and capillary electrophoresis-single-strand conformation polymorphisms. J. Virol. Methods 2012, 181, 139–147. [Google Scholar] [CrossRef]
- Scuderi, G.; Russo, M.; Davino, S.; Ferraro, R.; Catara, A.; Licciardello, G. Occurrence of the T36 Genotype of Citrus tristeza virus in Citrus Orchards in Sicily, Italy. Plant Dis. 2016, 100, 1253. [Google Scholar] [CrossRef]
- Licciardello, G.; Scuderi, G.; Ferraro, R.; Giampetruzzi, A.; Russo, M.; Lombardo, A.; Raspagliesi, D.; Bar-Joseph, M.; Catara, A. Deep sequencing and analysis of small RNAs in sweet orange grafted on sour orange infected with two citrus tristeza virus isolates prevalent in Sicily. Arch. Virol. 2015, 160, 2583–2589. [Google Scholar] [CrossRef]
- Müller, G.W.; Costa, A.S. Reduction in the yield of Galego lime avoided by preimmunization with mild strains of the tristeza virus. In Proceedings of the Fifth Conference of International Organization of Citrus Virologists; Price, W.C., Ed.; University of Florida Press: Gainesville, FL, USA, 1972; pp. 171–175. [Google Scholar]
- da Graça, J.V.; van Vuuren, S.P. Managing Citrus tristeza virus losses using cross protection. In Citrus Tristeza Virus Complex and Tristeza Diseases; Karasev, A.V., Hilf, M.E., Eds.; American Phytopathological Society: St. Paul, MN, USA, 2010; pp. 247–260. [Google Scholar]
- Luttig, M.; van Vuuren, S.P.; van der Vyver, J.B. Differentiation of single aphid cultured sub-isolates of two South African Citrus tristeza virus isolates from grapefruit by single-stranded conformation polymorphism. In Proceedings of the Fifteenth Conference of International Organization of Citrus Virologists; Duran-Vila, N., Milne, R.G., da Graça, J.V., Eds.; IOCV: Riverside, CA, USA, 2002; pp. 186–196. [Google Scholar]
- Roistacher, C.N.; da Graça, J.V.; Müller, G.W. Cross protection against Citrus tristeza virus—A review. In Proceedings of the Seventeenth Conference International Organization of Citrus Virologists; Hilf, M.E., Timmer, L.W., Milne, R.G., da Graça, J.V., Eds.; IOCV: Riverside, CA, USA, 2010; pp. 3–27. [Google Scholar]
- Ieki, H.; Yamaguchi, A.; Kano, T.; Koizumi, M.; Iwanami, T. Control of stem pitting caused by Citrus tristeza virus using protective mild strains in navel orange. Ann. Phytopathol. Soc. Jpn. 1997, 63, 170–175. [Google Scholar] [CrossRef]
- Lee, R.F.; Keremane, M.L. Mild strain cross protection of tristeza: A review of research to protect against decline on sour orange in Florida. Front. Microbiol. 2013, 4, 259. [Google Scholar] [CrossRef]
- Dawson, W.O.; Garnsey, S.M.; Tatineni, S.; Folimonova, S.Y.; Harper, S.J.; Gowda, S. Citrus tristeza virus-host interactions. Front. Microbiol. 2013, 4, 88. [Google Scholar] [CrossRef] [PubMed]
- Folimonova, S.Y.; Robertson, C.J.; Shilts, T.; Folimonov, A.S.; Hilf, M.E.; Garnsey, S.M.; Dawson, W.O. Infection with strains of Citrus tristeza virus does not exclude superinfection by other strains of the virus. J. Virol. 2010, 84, 1314–1325. [Google Scholar] [CrossRef] [PubMed]
- Folimonova, S.Y. Developing an understanding of cross-protection by citrus tristeza virus. Front. Microbiol. 2013, 4, 76. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.D.; Folimonova, S.Y. The p33 protein of Citrus tristeza virus affects viral pathogenicity by modulating a host immune response. New Phytol. 2019, 221, 2039–2053. [Google Scholar] [CrossRef]
- Folimonova, S.Y. Superinfection exclusion is an active virus-controlled function that requires a specific viral protein. J. Virol. 2012, 86, 5554–5561. [Google Scholar] [CrossRef]
- Tatineni, S.; French, R. The coat protein and NIa protease of two Potyviridae family members independently confer superinfection exclusion. J. Virol. 2016, 90, 23. [Google Scholar] [CrossRef]
- Harper, S.J.; Cowell, S.J.; Dawson, W.O. Isolate fitness and tissue-tropism determine superinfection success. Virology. 2017, 511, 222–228. [Google Scholar] [CrossRef] [PubMed]
- Bar-Joseph, M.; Catara, A.; Licciardello, G. The puzzling phenomenon of seedling yellows recovery and natural spread of asymptomatic infections of citrus tristeza virus: Two sides of the same coin. Hortic. Rev. 2021, 48, 7. [Google Scholar]
- Albiach-Martíì, M.R.; Robertson, C.J.; Gowda, S.; Tatineni, S.; Belliure, B.; Garnsey, S.M.; Folimonova, S.Y.; Moreno, P.; Dawson, W.O. The pathogenicity determinant of citrus tristeza virus causing the seedling yellows syndrome maps at the 3′-terminal region of the viral genome. Mol. Plant Pathol. 2010, 11, 55–67. [Google Scholar] [CrossRef]
- Cook, G.; van Vuuren, S.P.; Breytenbach, J.H.J.; Steyn, C.; Burger, J.T.; Maree, H.J. Characterization of Citrus tristeza virus single-variant sources in grapefruit in greenhouse and field trials. Plant Dis. 2016, 100, 2251–2256. [Google Scholar] [CrossRef] [PubMed]
- Cook, G.; Coetzee, B.; Bester, R.; Breytenbach, J.H.J.; Steyn, C.; de Bruyn, R.; Burger, J.; Maree, H. Citrus tristeza virus isolates of the same genotype differ in stem pitting severity in grapefruit. Plant Dis. 2020, 104, 2362–2368. [Google Scholar] [CrossRef]
- Harju, V.A.; Skelton, A.; Clover, G.R.G.; Ratti, C.; Boonham, N.; Henry, C.M.; Mumford, R.A. The use of real-time RT-PCR TaqMan (R) and post-ELISA virus release for the detection of beet necrotic yellow vein virus types containing RNA 5 and its comparison with conventional RT-PCR. J. Virol. Methods. 2005, 123, 73–80. [Google Scholar] [CrossRef]
- Ruiz-Ruiz, S.; Moreno, P.; Guerri, J.; Ambrós, S. Discrimination between mild and severe Citrus tristeza virus isolates with a rapid and highly specific real-time reverse transcription-polymerase chain reaction method using TaqMan LNA probes. Phytopathology. 2009, 99, 307–315. [Google Scholar] [CrossRef] [PubMed]
- Read, D.A.; Pietersen, G. Analysis of genotype composition of Citrus tristeza virus populations using Illumina Miseq technology. In Methods in Molecular Biology; Catara, A., Bar-Joseph, M., Licciardello, G., Eds.; Humana Press Inc.: New York, NY, USA, 2019; Volume 2015, pp. 179–194. [Google Scholar]
- Okonechnikov, K.; Conesa, A.; García-Alcalde, F. Qualimap 2: Advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics 2016, 32, 292–294. [Google Scholar] [CrossRef] [PubMed]
- Harper, S.J. Citrus tristeza virus: Evolution of complex and varied genotypic groups. Front. Microbiol. 2013, 4, 93. [Google Scholar] [CrossRef] [PubMed]
- Tamura, K.; Stecher, G.; Kumar, S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol. 2021, 38, 3022–3027. [Google Scholar] [CrossRef] [PubMed]
- Kearse, M.; Moir, R.; Wilson, A.; Stones-Havas, S.; Cheung, M.; Sturrock, S.; Buxton, S.; Cooper, A.; Markowitz, S.; Duran, C.; et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012, 28, 1647–1649. [Google Scholar] [CrossRef]
- Mawassi, M.; Mietkiewska, E.; Gofman, R.; Yang, G.; Bar-Joseph, M. Unusual sequence relationships between two isolates of Citrus tristeza virus. J. Gen. Virol. 1996, 77, 2359–2364. [Google Scholar] [CrossRef]
- Licciardello, G.; Ferraro, R.; Scuderi, G.; Russo, M.; Catara, A.F. A simulation of the use of high throughput sequencing as pre-screening assay to enhance the surveillance of citrus viruses and viroids in the EPPO Region. Agriculture 2021, 11, 400. [Google Scholar] [CrossRef]
- Pechinger, K.; Chooi, K.M.; MacDiarmid, R.M.; Harper, S.J.; Ziebell, H. A new era for mild strain cross-protection. Viruses 2019, 11, 670. [Google Scholar] [CrossRef]
- Folimonova, S.Y.; Achor, D.; Bar-Joseph, M. Walking together: Cross-protection, genome conservation, and the replication machinery of Citrus tristeza virus. Viruses 2020, 12, 1353. [Google Scholar] [CrossRef]
- Butković, A.; González, R. A brief view of factors that affect plant virus evolution. Front. Virol. 2022, 2, 994057. [Google Scholar] [CrossRef]
- Bar-Joseph, M.; Loebenstein, G. Effects of strain, source plant, and temperature on the transmissibility of citrus tristeza virus by the melon aphid. Phytopathology 1973, 63, 716–720. [Google Scholar] [CrossRef]
- Weng, Z.; Liu, X.; Gowda, S.; Barthelson, R.A.; Galbraith, D.W.; Dawson, W.O.; Xiong, Z. Extreme genome stability of citrus tristeza virus. In Proceedings of the Eighteenth Conference of International Organization of Citrus Virologists, Campinas, SP, Brazil, 7–12 November 2010. [Google Scholar]
- Silva, G.; Marques, N.; Nolasco, G. The evolutionary rate of citrus tristeza virus ranks among the rates of the slowest RNA viruses. J. Gen. Virol. 2012, 93, 419–429. [Google Scholar] [CrossRef] [PubMed]
- Kang, S.H.; Atallah, O.O.; Sun, Y.D.; Folimonova, S.Y. Functional diversification upon leader protease domain duplication in the Citrus tristeza virus genome: Role of RNA sequences and the encoded proteins. Virology 2018, 514, 192–202. [Google Scholar] [CrossRef]
- Atallah, O.O.; Kang, S.H.; El-Mohtar, C.A.; Shilts, T.; Bergua, M.; Folimonova, S.Y. A 5-proximal region of the Citrus tristeza virus genome encoding two leader proteases is involved in virus superinfection exclusion. Virology 2016, 489, 108–115. [Google Scholar] [CrossRef]
- Dao, T.N.M.; Kang, S.H.; Bak, A.; Folimonova, S.Y. A non-conserved p33 protein of Citrus tristeza virus interacts with multiple viral partners. Mol. Plant-Microbe Interact. 2020, 33, 859–870. [Google Scholar] [CrossRef]
- Bergua, M.; Zwart, M.P.; El-Mohtar, C.; Shilts, T.; Elena, S.F.; Folimonova, S.Y. A viral protein mediates superinfection exclusion at the whole-organism level but is not required for exclusion at the cellular level. J. Virol. 2014, 88, 11327–11338. [Google Scholar] [CrossRef]
- Sambade, A.; López, C.; Rubio, L.; Flores, R.; Guerri, J.; Moreno, P. Polymorphism of a specific region in gene p23 of citrus tristeza virus allows discrimination between mild and severe isolates. Arch. Virol. 2003, 148, 2325–2340. [Google Scholar] [CrossRef] [PubMed]
- Ruiz-Ruiz, S.; Navarro, B.; Pena, L.; Navarro, L.; Moreno, P.; Di Serio, F.; Flores, R. Citrus tristeza virus: Host RNA silencing and virus counteraction. In Methods in Molecular Biology; Catara, A., Bar-Joseph, M., Licciardello, G., Eds.; Humana Press Inc.: New York, NY, USA, 2019; Volume 2015, pp. 195–207. [Google Scholar]
- Nunna, H.; Qu, F.; Tatineni, S. P3 and NIa-Pro of Turnip Mosaic Virus Are Independent Elicitors of Superinfection Exclusion. Viruses 2023, 15, 1459. [Google Scholar] [CrossRef] [PubMed]
- Batuman, O.; Mawassi, M.; Bar-Joseph, M. Transgenes consisting of a dsRNA of an RNAi suppressor plus the 3′ UTR provide resistance to Citrus tristeza virus sequences in Nicotiana benthamiana but not in citrus. Virus Genes 2006, 33, 319–327. [Google Scholar] [PubMed]
- Dawson, W.O.; Bar-Joseph, M.; Garnsey, S.M.; Moreno, P. Citrus tristeza virus: Making an ally from an enemy. Ann. Rev. Phytopath. 2015, 53, 137–155. [Google Scholar] [CrossRef]
Source Trees | Age (yrs) | Location | CTV Isolate | Genotype and Phenotype | Mode of Infection |
---|---|---|---|---|---|
Alemow seedlings | 2 | Citrus nursery, Belpasso | Mac39 | VT no-SY | Aphid |
Mac101 | VT no-SY | Aphid | |||
M55 | VT no-SY | Aphid | |||
Duncan Gpf/TC | 2 | Greenhouse, Catania | M39D | VT no-SY | Inoculation |
Tarocco Lempso SwO/CC | 20 | Orchard, Lentini | Q7 | VT no-SY | UNK |
Moro SwO/SO | 30 | Orchard, Lentini | Nan1 | VT no-SY | UNK |
Moro SwO/SO | 30 | Orchard, Lentini | Nan2 | VT SY | UNK |
Pineapple SwO/CC | 1 | Greenhouse, Catania | P7(3C&4C) | VT SY | Inoculation |
Tarocco S.Alfio SwO/SO | 25 | Orchard, Scordia | P3R1 | VT SY | UNK |
Tarocco Tapi SwO/SO | 10 | Greenhouse, Catania | Tapi | VT SY | Inoculation |
CP Isolate | SY Isolate | Host Plant | CP Inoculation | SY Inoculation | No. of Plants | |
---|---|---|---|---|---|---|
CP | CP + SY | |||||
Long term trials | ||||||
M39D | None | SO | October 2014 | // | 6 | // |
Mac39 | P7/4C | SO | October 2014 | February 2021 | 2 | 4 |
Mac39 | P3R1 | H SwO/Ale | October 2014 | October 2021 | 4 | 6 |
Mac101 | P3R1 | H SwO/SO | October 2014 | October 2021 | 2 | 4 |
Short term trials | ||||||
M39D | P7/3C | SO | June 2020 | May 2021 | 4 | 4 |
Mac101 | P7/3C | SO | June 2020 | May 2021 | 4 | 4 |
Q7 | P7/3C | T SwO/SO | June 2020 | September 2021 | 5 | 5 |
M39D | P7/3C | H SwO/SO | June 2020 | August 2021 | 5 | 5 |
M55 | Tapi | SO | June 2020 | September 2021 | 2 | 4 |
Nan1 | P3R1 | SO | June 2020 | September 2021 | 2 | 4 |
Nan1 | Tapi | SO | June 2020 | October 2021 | 2 | 4 |
Sample | Reads Number | CTV Isolate Reference Genomes (Reads/Coverage) | ||||||
---|---|---|---|---|---|---|---|---|
VT KC748392 | VT No-SY KJ790175 | T30 KC748391 | RB FJ525435 | T36 EU937521 | T3 EU857538 | B165 EU076703 | ||
M39D | 11.64 M | 1.23 M 100% | 1.34 M 100% | 482.907 75% | 376.301 65% | 385.023 55% | 1.06 M 80% | 1.05 M 80% |
Nan1 | 17.05 M | 3.05 M 100% | 3.17 M 100% | 649.833 74% | 526.440 67% | 495.293 60% | 1.28 M 85% | 1.32 M 85% |
Q7 | 22.73 M | 2.24 M 100% | 2.56 M 100% | 762.004 75% | 736.293 65% | 561.395 55% | 1.57 M 80% | 1.98 M 80% |
M55 | 51.32 M | 2.82 M 100% | 2.81 M 100% | 761.194 75% | 587.717 65% | 546.631 60% | 1.07 M 85% | 1.55 M 85% |
Isolate | GenBank 1 | Phenotype | Orf1a 3 | P33 | P23 | |||||
---|---|---|---|---|---|---|---|---|---|---|
486 nt 127 aa | 815 nt 236 aa | 3578 nt 1157 aa | 4873 nt 1589 aa | 11,490 nt 210 aa | 11,585 nt 242 aa | 11,756 nt 299 aa | 18,508 nt 54 aa | |||
SG29 | KC748392 | SY | T/Phe | C/Asp | C/Asp | T/Iso | G/Pro | C/Ala | G/Gly | G/Ser |
P3R1 | / 2 | SY | T/Phe | C/Asp | C/Asp | T/Iso | G/Pro | C/Ala | G/Gly | G/Ser |
Mac39 | KJ790175 | No-SY | A/Ile | T/Asp | T/Asp | C/Thr | A/Pro | T/Val | A/Ala | A/Asn |
Mac101 | MW689620 | No-SY | A/Ile | T/Asp | T/Asp | C/Thr | A/Pro | T/Val | A/Ala | A/Asn |
M39D | OR387854 | No-SY | A/Ile | T/Asp | T/Asp | C/Thr | A/Pro | T/Val | A/Ala | A/Asn |
M55 | OP345183 | No-SY | A/Ile | T/Asp | T/Asp | C/Thr | A/Pro | T/Val | A/Ala | A/Asn |
Q7 | OM803129 | No-SY | A/Ile | T/Asp | T/Asp | C/Thr | A/Pro | T/Val | A/Ala | A/Asn |
Nan1 | OP345182 | No-SY | A/Ile | T/Asp | T/Asp | C/Thr | A/Pro | T/Val | A/Ala | A/Asn |
Isolates | Sequencing | Host | Phenotype | p33 | p23 | ||
---|---|---|---|---|---|---|---|
630 nt (11,490 nt) | 725 nt (11,585 nt) | 896 nt (11,756 nt) | 161 nt (18,508 nt) | ||||
SG29 * | HTS | SwO | SY | G | C | G | G |
P7 | Sanger | SwO | SY | A | T | C | G |
P3R1 | HTS | SwO | SY | G | C | G | G |
Nan2 | Sanger | SO | SY | A | T | C | G |
Mac39 | HTS | Alem | no-SY | A | T | C | A |
Sanger | Alem | no-SY | A | T | C | A | |
M39.12 | Sanger | Alem | no-SY | A | T | C | A |
M39D | HTS | Gpf | no-SY | A | T | C | A |
Sanger | Gpf | no-SY | A | T | C | A | |
Mac101 Mac10 | HTS | Alem | no-SY | A | T | C | A |
Sanger | Gpf | no-SY | A | T | C | A | |
M55 | HTS | SO | no-SY | A | T | C | A |
Sanger | SO | no-SY | A | T | C | A | |
Sanger | Citr | no-SY | A | T | C | A | |
Q7 | HTS | SwO | no-SY | A | T | C | A |
Sanger | SwO | no-SY | A | T | C | A | |
Nan1 | HTS | SO | no-SY | A | T | C | A |
Sanger | SO | no-SY | A | T | C | A |
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Licciardello, G.; Scuderi, G.; Russo, M.; Bazzano, M.; Bar-Joseph, M.; Catara, A.F. Minor Variants of Orf1a, p33, and p23 Genes of VT Strain Citrus Tristeza Virus Isolates Show Symptomless Reactions on Sour Orange and Prevent Superinfection of Severe VT Isolates. Viruses 2023, 15, 2037. https://doi.org/10.3390/v15102037
Licciardello G, Scuderi G, Russo M, Bazzano M, Bar-Joseph M, Catara AF. Minor Variants of Orf1a, p33, and p23 Genes of VT Strain Citrus Tristeza Virus Isolates Show Symptomless Reactions on Sour Orange and Prevent Superinfection of Severe VT Isolates. Viruses. 2023; 15(10):2037. https://doi.org/10.3390/v15102037
Chicago/Turabian StyleLicciardello, Grazia, Giuseppe Scuderi, Marcella Russo, Marina Bazzano, Moshe Bar-Joseph, and Antonino F. Catara. 2023. "Minor Variants of Orf1a, p33, and p23 Genes of VT Strain Citrus Tristeza Virus Isolates Show Symptomless Reactions on Sour Orange and Prevent Superinfection of Severe VT Isolates" Viruses 15, no. 10: 2037. https://doi.org/10.3390/v15102037
APA StyleLicciardello, G., Scuderi, G., Russo, M., Bazzano, M., Bar-Joseph, M., & Catara, A. F. (2023). Minor Variants of Orf1a, p33, and p23 Genes of VT Strain Citrus Tristeza Virus Isolates Show Symptomless Reactions on Sour Orange and Prevent Superinfection of Severe VT Isolates. Viruses, 15(10), 2037. https://doi.org/10.3390/v15102037