Serological and Molecular Detection of Citrus Tristeza Virus: A Review
Abstract
:1. Introduction
2. Pathogen and Symptomatology
3. Immunological Methods
3.1. ELISA
3.2. DTBIA
3.3. LFIA
3.4. Immuno-Electron Microscopy
4. Nucleic Acid-Based Detection Methods
4.1. Conventional RT-PCR/RT-qPCR
Type | Advantages | Limitations | Sample Type | Gene Targeted | Characteristics | References |
---|---|---|---|---|---|---|
RT-qPCR | Commercially available More sensitive than cPCR Quantitative analyses | Sophisticated equipment is required Tedious procedure Comparatively higher cost | Total RNA | ORFs 1b and ORFs 2; CP | Quantitatively analyzes CTV content. | [85,86] |
TP-RT-PCR | No need to extract nucleic acids Convenient for storage and transportation Removes inhibitors efficiently | Sophisticated equipment is required Low RNA content limits its sensitivity | Pieces of membrane harboring the printed samples | 3′ UTR and CP | IPPC-FAO standard recommendations. | [69] |
Multiplex RT-PCR | Distinguish co-infections Low cost | Sophisticated equipment is required Susceptible to non-specific amplification | Total RNA | 5′UTR, ORF1a, ORF1b, p33, p20, and p23. | Six genotypes were distinguished. | [90] |
Nested RT-PCR | No need to extract nucleic acids Low cost | Lower sensitivity than real-time RT-PCR and DAS-ELISA | Crude leaf sap | 3′UTR | The sensitivity higher than cPCR, but lower than RT-qPCR and DAS-ELISA. | [78] |
RT-ddPCR | Higher accuracy than RT-qPCR Without need for a standard curve Increased tolerance to inhibitors | Limited upper limits may lead to signal saturation Comparatively higher cost | Total RNA | CP | 100-fold greater sensitivity than RTqPCR. | [91] |
RT-LAMP | No need to extract nucleic acids The detection time is short Low requirements for instruments Result visualization | Difficult to quantify Complex primer design | Total RNA | CP | The minimum amplification time was 6:45 (min:s) | [92] |
SSCP | Low requirements for instruments Low cost | Difficult to quantify Limited analytical ability | Total RNA | CP | Screening of mild strains for cross-protection | [93] |
4.2. TP-RT-PCR
4.3. Multiplex RT-PCR
4.4. Nested RT-PCR
4.5. Digital Droplet PCR
4.6. RT-LAMP
4.7. Single-Strand Conformation Polymorphism Analysis (SSCP)/Capillary Electrophoresis SSCP (CE-SSCP)
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- 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. [Google Scholar] [CrossRef] [PubMed]
- Cook, G.; Breytenbach, J.H.; Steyn, C.; de Bruyn, R.; van Vuuren, S.P.; Burger, J.T.; Maree, H.J. Grapefruit field trial evaluation of Citrus tristeza virus T68-strain sources. Plant Dis. 2021, 105, 361–367. [Google Scholar] [CrossRef] [PubMed]
- Moreno, P.; Ambrós, S.; Albiach-Martí, M.R.; Guerri, J.; Pena, L. Citrus tristeza virus: A pathogen that changed the course of the citrus industry. Mol. Plant Pathol. 2008, 9, 251–268. [Google Scholar] [CrossRef] [PubMed]
- Folimonova, S.Y.; Sun, Y.-D. Citrus Tristeza Virus: From Pathogen to Panacea. Annu. Rev. Virol. 2022, 9, 417–435. [Google Scholar] [CrossRef] [PubMed]
- Abbas, Z.; Hameed, S.; Lockhart, B.; Bratsch, S.; Olszewski, N.; Rehman, M.; Saqlan Naqvi, S. Production and evaluation of polyclonal antibodies against homologous Citrus tristeza virus (CTV) isolates from Pakistan. JAPS J. Anim. Plant Sci. 2021, 31, 1052–1059. [Google Scholar]
- Bester, R.; Cook, G.; Maree, H.J. Citrus tristeza virus genotype detection using high-throughput sequencing. Viruses 2021, 13, 168. [Google Scholar] [CrossRef] [PubMed]
- Folimonova, S.Y. Citrus tristeza virus: A large RNA virus with complex biology turned into a valuable tool for crop protection. PLoS Pathog. 2020, 16, e1008416. [Google Scholar] [CrossRef]
- Ayllón, M.A.; Gowda, S.; Satyanarayana, T.; Dawson, W.O. cis-acting elements at opposite ends of the Citrus tristeza virus genome differ in initiation and termination of subgenomic RNAs. Virology 2004, 322, 41–50. [Google Scholar] [CrossRef]
- Iftikhar, Y.; Abbas, M.; Mubeen, M.; Zafar-ul-Hye, M.; Bakhtawar, F.; Bashir, S.; Sajid, A.; Shabbir, M.A. Overview of Strain Characterization in Relation to Serological and Molecular Detection of Citrus tristeza Closterovirus. Phyton-Int. J. Exp. Bot 2021, 90, 1063–1074. [Google Scholar] [CrossRef]
- Karasev, A.; Boyko, V.; Gowda, S.; Nikolaeva, O.; Hilf, M.; Koonin, E.; Niblett, C.; Cline, K.; Gumpf, D.; Lee, R. Complete sequence of the citrus tristeza virus RNA genome. Virology 1995, 208, 511–520. [Google Scholar] [CrossRef]
- Dawson, W.O.; Bar-Joseph, M.; Garnsey, S.M.; Moreno, P. Citrus tristeza virus: Making an ally from an enemy. Annu. Rev. Phytopathol. 2015, 53, 137–155. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.D.; Folimonova, S.Y. Location matters: From changing a presumption about the Citrus tristeza virus tissue tropism to understanding the stem pitting disease. New Phytol. 2022, 233, 631–638. [Google Scholar] [CrossRef] [PubMed]
- Febres, V.; Ashoulin, L.; Mawassi, M.; Frank, A.; Bar-Joseph, M.; Manjunath, K.; Lee, R.; Niblett, C. The p27 protein is present at one end of citrus tristeza virus particles. Phytopathology 1996, 86, 1331–1335. [Google Scholar]
- Sekiya, M.E.; Lawrence, S.D.; McCaffery, M.; Cline, K. Molecular cloning and nucleotide sequencing of the coat protein gene of citrus tristeza virus. J. Gen. Virol. 1991, 72, 1013–1020. [Google Scholar] [CrossRef] [PubMed]
- Shangguan, C.; Kuang, Y.; Chen, Z.; Yu, X. Screening candidate effectors from the salivary gland transcriptomes of brown citrus aphid, Aphis citricidus. Arthropod-Plant Interact. 2024, 1–11. [Google Scholar] [CrossRef]
- Paiva, P.E.B.; Neto, L.M.; Marques, N.T.; Duarte, B.Z.; Duarte, A.M. Citrus Aphids in Algarve Region (Portugal): Species, Hosts, and Biological Control. Ecologies 2024, 5, 101–115. [Google Scholar] [CrossRef]
- Korkmaz, S.; Karanfil, A.; Satar, S.; Uslu, T.; Koç, N.K.; Çevik, B. Effects of graft and aphid transmission on the genetic diversity and population structure of Turkish citrus tristeza virus isolates. Eur. J. Plant Pathol. 2022, 162, 369–388. [Google Scholar] [CrossRef]
- Albertini, D.; Vogel, R.; Bové, C.; Bové, J. Transmission and Preliminary Characterization of Citrus Tristeza Virus Strain. Int. Organ. Citrus Virol. Conf. Proc. (1957–2010) 1988, 10, 17–21. [Google Scholar] [CrossRef]
- Chen, Y.; Yi, L.; Zhong, K.; Wang, C.; Chen, B.; Li, S. Population genetic characteristics of citrus tristeza virus from wild mandarins in the Nanling Mountains of China. Trop. Plant Pathol. 2023, 48, 270–282. [Google Scholar] [CrossRef]
- Roistacher, C.; Bar-Joseph, M. Aphid transmission of citrus tristeza virus: A review. Phytophylactica 1987, 19, 163–168. [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]
- EFSA Panel on Plant Health (PLH); Jeger, M.; Bragard, C.; Caffier, D.; Candresse, T.; Chatzivassiliou, E.; Dehnen-Schmutz, K.; Gilioli, G.; Grégoire, J.-C.; Jaques Miret, J.A.; et al. Pest categorisation of Toxoptera citricida. EFSA J. 2018, 16, e05103. [Google Scholar]
- Garnsey, S.M.; Civerolo, E.L.; Gumpf, D.J.; Paul, C.; Hartung, J.S. Biological Characterization of an International Collection of Citrus tristeza virus (CTV) Isolates. Int. Organ. Citrus Virol. Conf. Proc. (1957–2010) 2005, 16, 75–93. [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]
- Gonsalves, D.; Purcifull, D.; Garnsey, S. Purification and serology of citrus tristeza virus. Phytopathology 1978, 68, 553–559. [Google Scholar] [CrossRef]
- Lbida, B.; Bennani, A.; Serrhini, M.N.; Zemzami, M. Biological, serological and molecular characterization of three isolates of Citrus tristeza closterovirus introduced into Morocco. EPPO Bull. 2005, 35, 511–517. [Google Scholar] [CrossRef]
- Jeger, M.; Bragard, C.; Caffier, D.; Dehnen-Schmutz, K.; Gilioli, G.; Gregoire, J.C.; Jaques Miret, J.A.; Macleod, A.; Navajas Navarro, M.; Niere, B. Pest categorisation of Citrus tristeza virus (non-European isolates). EFSA J. 2017, 15, e05031. [Google Scholar]
- López, M.M.; Bertolini, E.; Olmos, A.; Caruso, P.; Gorris, M.T.; Llop, P.; Penyalver, R.; Cambra, M. Innovative tools for detection of plant pathogenic viruses and bacteria. Int. Microbiol. 2003, 6, 233–243. [Google Scholar] [CrossRef]
- Fang, Y.; Ramasamy, R.P. Current and prospective methods for plant disease detection. Biosensors 2015, 5, 537–561. [Google Scholar] [CrossRef] [PubMed]
- Venbrux, M.; Crauwels, S.; Rediers, H. Current and emerging trends in techniques for plant pathogen detection. Front. Plant Sci. 2023, 14, 25. [Google Scholar] [CrossRef]
- Brlansky, R.; Garnsey, S.; Lee, R.; Purcifull, D. Application of citrus tristeza virus antisera in labeled antibody, immuno-electron microscopical and sodium dodecyl immunodiffusion tests. Int. Organ. Citrus Virol. Conf. Proc. (1957–2010) 1984, 9. [Google Scholar] [CrossRef]
- Maheshwari, Y.; Selvaraj, V.; Hajeri, S.; Ramadugu, C.; Keremane, M.L.; Yokomi, R.K. On-site detection of Citrus tristeza virus (CTV) by lateral flow immunoassay using polyclonal antisera derived from virions produced by a recombinant CTV. Phytoparasitica 2017, 45, 333–340. [Google Scholar] [CrossRef]
- Raeisi, H.; Safarnejad, M.R.; Sadeghkhani, F. A new single-chain variable fragment (scFv) antibody provides sensitive and specific detection of citrus tristeza virus. J. Virol. Methods 2022, 300, 114412. [Google Scholar] [CrossRef] [PubMed]
- Robison, B.J. Use of commercially available ELISA kits for detection of foodborne pathogens. In Diagnostic Bacteriology Protocols; Humana Press: Totowa, NJ, USA, 1995; Volume 46, pp. 123–132. [Google Scholar]
- Nikolaeva, O.V.; Karasev, A.V.; Garnsey, S.M.; Lee, R.F. Serological differentiation of the citrus tristeza virus isolates causing stem fitting in sweet orange. Plant Dis. 1998, 82, 1276–1280. [Google Scholar] [CrossRef] [PubMed]
- Nikolaeva, O.; Karasev, A.; Powell, C.; Gumpf, D.; Garnsey, S.; Lee, R. Mapping of epitopes for citrus tristeza virus-specific monoclonal antibodies using bacterially expressed coat protein fragments. Phytopathology 1996, 86, 974–979. [Google Scholar] [CrossRef]
- Shokri, E.; Hosseini, M.; Sadeghan, A.A.; Bahmani, A.; Nasiri, N.; Hosseinkhani, S. Virus-directed synthesis of emitting copper nanoclusters as an approach to simple tracer preparation for the detection of Citrus Tristeza Virus through the fluorescence anisotropy immunoassay. Sens. Actuators B Chem. 2020, 321, 128634. [Google Scholar] [CrossRef]
- Alvarez, A.M. Integrated approaches for detection of plant pathogenic bacteria and diagnosis of bacterial diseases. Annu. Rev. Phytopathol 2004, 42, 339–366. [Google Scholar] [CrossRef] [PubMed]
- Martinelli, F.; Scalenghe, R.; Davino, S.; Panno, S.; Scuderi, G.; Ruisi, P.; Villa, P.; Stroppiana, D.; Boschetti, M.; Goulart, L.R. Advanced methods of plant disease detection. A review. Agron. Sustain. Dev. 2015, 35, 1–25. [Google Scholar] [CrossRef]
- Ascoli, C.A.; Aggeler, B. Overlooked benefits of using polyclonal antibodies. Biotechniques 2018, 65, 127–136. [Google Scholar] [CrossRef]
- Cambra, M.; Gorris, M.; Román, M.; Terrada, E.; Garnsey, S.; Camarasa, E.; Olmos, A.; Colomer, M. Routine detection of citrus tristeza virus by direct immunoprinting-ELISA method using specific monoclonal and recombinant antibodies. Int. Organ. Citrus Virol. Conf. Proc. (1957–2010) 2000, 14, 34–41. [Google Scholar] [CrossRef]
- Posthuma-Trumpie, G.A.; Korf, J.; van Amerongen, A. Lateral flow (immuno) assay: Its strengths, weaknesses, opportunities and threats. A literature survey. Anal. Bioanal. Chem. 2009, 393, 569–582. [Google Scholar] [CrossRef] [PubMed]
- Kumar, A.; Singh, U.; Kumar, J.; Garg, G. Application of molecular and immuno-diagnostic tools for detection, surveillance and quarantine regulation of Karnal bunt (Tilletia indica) of wheat. Food Agric. Immunol. 2008, 19, 293–311. [Google Scholar] [CrossRef]
- Atmar, R.L. Immunological detection and characterization. In Viral Infections of Humans: Epidemiology and Control; Springer: Berlin/Heidelberg, Germany, 2014; pp. 47–62. [Google Scholar]
- Sakamoto, S.; Putalun, W.; Vimolmangkang, S.; Phoolcharoen, W.; Shoyama, Y.; Tanaka, H.; Morimoto, S. Enzyme-linked immunosorbent assay for the quantitative/qualitative analysis of plant secondary metabolites. J. Nat. Med. 2018, 72, 32–42. [Google Scholar] [CrossRef] [PubMed]
- Magdalena Iracheta-Cárdenas, M.; Alberto Rocha-Peña, M. Comparación de Antisueros Comerciales para la Detección del Virus Tristeza de los Cítricos. Rev. Mex. Fitopatol. 2005, 23, 323. [Google Scholar]
- Llanes-Alvarez, Y.; Peña-Bárzaga, I.; Batista-Le Riverend, L.; Pacheco, R.; Zamora-Rodríguez, V.; Benítez-Galeano, M.J.; Rivas, F.; Bertalmío, A.; Hernández-Rodríguez, L. Prevalence of mild citrus tristeza virus isolates of the T30 genotype in Cuban commercial citrus fields after the dissemination of huanglongbing. Crop Prot. 2021, 140, 105422. [Google Scholar] [CrossRef]
- Biswas, K. Molecular diagnosis of Citrus tristeza virus in mandarin (Citrus reticulata) orchards of Darjeeling hills of West Bengal. Indian J. Virol. 2008, 19, 26–31. [Google Scholar]
- Biswas, K.; Tarafdar, A.; Sharma, S.; Singh, J.; Dwivedi, S.; Biswas, K.; Jayakumar, B. Current status of Citrus tristeza virus incidence and its spatial distribution in citrus growing geographical zones of India. Indian J. Agric. Sci. 2014, 84, 184–189. [Google Scholar] [CrossRef]
- Moreno, P.; Cambra, M.; Navarro, L.; Fernandez Montes, J.; Pina, J.A.; Ballester, J.F.; Juarez, J. A Survey of Citrus Tristeza Virus (CTV) in the Area of Sevilla (Spain) Using the ELISA Method. 1980. Available online: https://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=PASCALAGROLINEINRA8110459313 (accessed on 20 May 2024).
- Vela, C.; Cambra, M.; Cortés, E.; Moreno, P.; Miguet, J.; Pérez de San Román, C.; Sanz, A. Production and characterization of monoclonal antibodies specific for citrus tristeza virus and their use for diagnosis. J. Gen. Virol. 1986, 67, 91–96. [Google Scholar] [CrossRef]
- Cambra, M. Historias de la Inmunología/Serología en España contadas por un fitopatólogo. Fitopatología 2018, 43–54. Available online: http://hdl.handle.net/20.500.11939/7839 (accessed on 20 May 2024).
- Cambra, M.; Gorris, M.T.; Marroquın, C.; Román, M.P.; Olmos, A.; Martınez, M.C.; de Mendoza, A.H.; Lopez, A.; Navarro, L. Incidence and epidemiology of Citrus tristeza virus in the Valencian Community of Spain. Virus Res. 2000, 71, 85–95. [Google Scholar] [CrossRef]
- Cambra, M.; Camarasa, E.; Gorris, M.; Garnsey, S.; Carbonell, E. Comparison of different immunosorbent assays for citrus tristeza virus (CTV) using CTV specific monoclonal and polyclonal antibodies. Int. Organ. Citrus Virol. Conf. Proc. (1957–2010) 1991, 11, 38–45. [Google Scholar] [CrossRef]
- Cambra, M.; Garnsey, S.; Permar, T.; Henderson, C.; Gumpf, D.; Vela, C. Detection of citrus tristeza virus (CTV) with a mixture of monoclonal antibodies. Phytopathology 1990, 80, 1034. [Google Scholar]
- Liu, Z.; Chen, Z.; Hong, J.; Wang, X.; Zhou, C.; Zhou, X.; Wu, J. Monoclonal antibody-based serological methods for detecting Citrus tristeza virus in citrus groves. Virol. Sin. 2016, 31, 324–330. [Google Scholar] [CrossRef]
- Terrada, E.; Kerschbaumer, R.J.; Giunta, G.; Galeffi, P.; Himmler, G.; Cambra, M. Fully “recombinant enzyme-linked immunosorbent assays” using genetically engineered single-chain antibody fusion proteins for detection of Citrus tristeza virus. Phytopathology 2000, 90, 1337–1344. [Google Scholar] [CrossRef] [PubMed]
- Permar, T.; Garnsey, S.; Gumpf, D.; Lee, R. A monoclonal antibody that discriminates strains of citrus tristeza virus. Phytopathology 1990, 80, 224–228. [Google Scholar] [CrossRef]
- KORKMAZ, S. Application of direct tissue blot immunoassay in comparison with DAS-ELISA for detection of Turkish isolates of citrus tristeza closterovirus (CTV). Turk. J. Agric. For. 2002, 26, 203–209. [Google Scholar]
- Rocha-Peña, M.A.; Lee, R.F. Serological techniques for detection of citrus tristeza virus. J. Virol. Methods 1991, 34, 311–331. [Google Scholar] [CrossRef]
- Garnsey, S.; Permar, T.; Cambra, M.; Henderson, C. Direct tissue blot immunoassay (DTBIA) for detection of citrus tristeza virus (CTV). Int. Organ. Citrus Virol. Conf. Proc. (1957–2010) 1993, 12, 39–50. [Google Scholar] [CrossRef]
- Powell, C.; Pelosi, R.; Rundell, P.; Stover, E.; Cohen, M. Cross-protection of grapefruit from decline-inducing isolates of citrus tristeza virus. Plant Dis. 1999, 83, 989–991. [Google Scholar] [CrossRef]
- Lin, Y.; Rundell, P.A.; Xie, L.; Powell, C.A. In situ immunoassay for detection of Citrus tristeza virus. Plant Dis. 2000, 84, 937–940. [Google Scholar] [CrossRef]
- Cevik, B.; Pappu, S.; Pappu, H.; Benscher, D.; Irey, M.; Lee, R.; Niblett, C. Application of bi-directional PCR to citrus tristeza virus: Detection and strain differentiation. Int. Organ. Citrus Virol. Conf. Proc. (1957–2010) 1996, 13, 17–24. [Google Scholar] [CrossRef]
- Kano, T.; Hiyama, T.; Natsuaki, T.; Imanishi, N.; Okuda, S.; Ieki, H. Comparative sequence analysis of biologically distinct isolates of citrus tristeza virus in Japan. Jpn. J. Phytopathol. 1998, 64, 270–275. [Google Scholar] [CrossRef]
- Pappu, H.; Pappu, S.; Manjunath, K.; Lee, R.; Niblett, C. Molecular characterization of a structural epitope that is largely conserved among severe isolates of a plant virus. Proc. Natl. Acad. Sci. USA 1993, 90, 3641–3644. [Google Scholar] [CrossRef] [PubMed]
- Cambra, M.; Camarasa, E.; Gorris, M.; Román, M. Distribución actual de la tristeza de los cítricos y nuevos métodos de diagnóstico. Phytoma 1994, 72, 150–158. [Google Scholar]
- Cambra, M.; Gorris, M.T.; Camarasa, E.; Román, M.; Narváez, G.; Terrada, E.; Martínez, M.C. Inmunoimpresión-ELISA: Método ideal para detección del virus de la tristeza de los cítricos. Comunitat Valencia. Agrar. 1999, 13, 4–14. Available online: http://hdl.handle.net/20.500.11939/7588 (accessed on 20 May 2024).
- Cambra, M.; Vidal, E.; Martinez, C.; Bertolini, E. Tissue-Print and Squash Capture Real-Time RT-PCR Method for Direct Detection of Citrus tristeza virus (CTV) in Plant or Vector Tissues. In Citrus Tristeza Virus: Methods and Protocols; Catara, A.F., BarJoseph, M., Licciardello, G., Eds.; Humana Press Inc.: Totowa, NJ, USA, 2019; Volume 2015, pp. 55–66. [Google Scholar]
- Lopez-Soriano, P.; Noguera, P.; Gorris, M.T.; Puchades, R.; Maquieira, A.; Marco-Noales, E.; López, M.M. Lateral flow immunoassay for on-site detection of Xanthomonas arboricola pv. pruni in symptomatic field samples. PLoS ONE 2017, 12, e0176201. [Google Scholar] [CrossRef] [PubMed]
- Salomone, A.; Mongelli, M.; Roggero, P.; Boscia, D. Reliability of detection of Citrus tristeza virus by an immunochromatographic lateral flow assay in comparison with ELISA. J. Plant Pathol. 2004, 86, 43–48. [Google Scholar]
- Ahmed, S.; Ning, J.; Peng, D.; Chen, T.; Ahmad, I.; Ali, A.; Lei, Z.; Abu bakr Shabbir, M.; Cheng, G.; Yuan, Z. Current advances in immunoassays for the detection of antibiotics residues: A review. Food Agric. Immunol. 2020, 31, 268–290. [Google Scholar] [CrossRef]
- Koczula, K.M.; Gallotta, A. Lateral flow assays. Essays Biochem. 2016, 60, 111–120. [Google Scholar]
- Schneider, H. The anatomy of tristeza-virus-infected citrus. Int. Organ. Citrus Virol. Conf. Proc. (1957–2010) 1957, 1, 73–84. [Google Scholar] [CrossRef]
- Garnsey, S.; Christie, R.; Derrick, K.; Bar-Joseph, M. Detection of citrus tristeza virus. II. Light and electron microscopy of inclusions and viral particles. Int. Organ. Citrus Virol. Conf. Proc. (1957–2010) 1980, 8, 9–15. [Google Scholar] [CrossRef]
- Brlansky, R.; Howd, D.; Broadbent, P.; Damsteegt, V. Histology of sweet orange stem pitting caused by an Australian isolate of Citrus tristeza virus. Plant Dis. 2002, 86, 1169–1174. [Google Scholar] [CrossRef] [PubMed]
- Folimonova, S.Y.; Folimonov, A.S.; Tatineni, S.; Dawson, W.O. Citrus tristeza virus: Survival at the edge of the movement continuum. J. Virol. 2008, 82, 6546–6556. [Google Scholar] [CrossRef] [PubMed]
- Bertolini, E.; Moreno, A.; Capote, N.; Olmos, A.; de Luis, A.; Vidal, E.; Pérez-Panadés, J.; Cambra, M. Quantitative detection of Citrus tristeza virus in plant tissues and single aphids by real-time RT-PCR. Eur. J. Plant Pathol. 2008, 120, 177–188. [Google Scholar] [CrossRef]
- Cook, G.; van Vuuren, S.P.; Breytenbach, J.H.; Burger, J.T.; Maree, H.J. Expanded strain-specific RT-PCR assay for differential detection of currently known citrus tristeza virus strains: A useful screening tool. J. Phytopathol. 2016, 164, 847–851. [Google Scholar] [CrossRef]
- Ward, E.; Foster, S.J.; Fraaije, B.A.; Mccartney, H.A. Plant pathogen diagnostics: Immunological and nucleic acid-based approaches. Ann. Appl. Biol. 2004, 145, 1–16. [Google Scholar] [CrossRef]
- López, M.M.; Llop, P.; Olmos, A.; Marco-Noales, E.; Cambra, M.; Bertolini, E. Are molecular tools solving the challenges posed by detection of plant pathogenic bacteria and viruses? Curr. Issues Mol. Biol. 2009, 11, 13–46. [Google Scholar] [CrossRef]
- Maurer, J.J. Rapid detection and limitations of molecular techniques. Annu. Rev. Food Sci. Technol. 2011, 2, 259–279. [Google Scholar] [CrossRef] [PubMed]
- Singh, C.; Roy-Chowdhuri, S. Quantitative Real-Time PCR: Recent Advances. In Clinical Applications of PCR; Luthra, R., Singh, R.R., Patel, K.P., Eds.; Springer: New York, NY, USA, 2016; pp. 161–176. [Google Scholar]
- Shen, C. Chapter 9—Amplification of Nucleic Acids. In Diagnostic Molecular Biology; Shen, C., Ed.; Academic Press: Cambridge, MA, USA, 2019; pp. 215–247. [Google Scholar] [CrossRef]
- Ruiz-Ruiz, S.; Moreno, P.; Guerri, J.; Ambrós, S. A real-time RT-PCR assay for detection and absolute quantitation of Citrus tristeza virus in different plant tissues. J. Virol. Methods 2007, 145, 96–105. [Google Scholar] [CrossRef]
- Saponari, M.; Manjunath, K.; Yokomi, R.K. Quantitative detection of Citrus tristeza virus in citrus and aphids by real-time reverse transcription-PCR (TaqMan®). J. Virol. Methods 2008, 147, 43–53. [Google Scholar] [CrossRef] [PubMed]
- Mirmajlessi, S.M.; Loit, E.; Maend, M.; Mansouripour, S.M. Real-time PCR applied to study on plant pathogens: Potential applications in diagnosis-a review. Plant Prot. Sci. 2015, 51, 177–190. [Google Scholar] [CrossRef]
- Okubara, P.A.; Schroeder, K.L.; Paulitz, T.C. Real-time polymerase chain reaction: Applications to studies on soilborne pathogens. Can. J. Plant Pathol. 2005, 27, 300–313. [Google Scholar] [CrossRef]
- Liu, J.; Li, L.; Zhao, H.; Zhou, Y.; Wang, H.; Li, Z.; Zhou, C. Titer variation of citrus tristeza virus in aphids at different acquisition access periods and its association with transmission efficiency. Plant Dis. 2019, 103, 874–879. [Google Scholar] [CrossRef] [PubMed]
- Scuderi, G.; Catara, A.F.; Licciardello, G. Genotyping Citrus tristeza virus Isolates by Sequential Multiplex RT-PCR and Microarray Hybridization in a Lab-on-Chip Device. In Citrus Tristeza Virus: Methods and Protocols; Catara, A.F., BarJoseph, M., Licciardello, G., Eds.; Humana Press Inc.: Totowa, NJ, USA, 2019; Volume 2015, pp. 127–142. [Google Scholar]
- Wang, Y.; Yang, Z.; Zhao, J.; Li, R.; Wang, Q.; Li, J.; Li, Z.; Zhou, Y. Development of a sensitive and reliable reverse transcription-droplet digital polymerase chain reaction (RT-ddPCR) assay for the detection of Citrus tristeza virus. Eur. J. Plant Pathol. 2020, 156, 1175–1180. [Google Scholar] [CrossRef]
- Selvaraj, V.; Maheshwari, Y.; Hajeri, S.; Yokomi, R. A rapid detection tool for VT isolates of Citrus tristeza virus by immunocapture-reverse transcriptase loop-mediated isothermal amplification assay. PLoS ONE 2019, 14, e0222170. [Google Scholar] [CrossRef] [PubMed]
- Atta, S.; Umar, U.u.d.; Bashir, M.A.; Hannan, A.; Rehman, A.u.; Naqvi, S.A.H.; Zhou, C. Application of biological and single-strand conformation polymorphism assays for characterizing potential mild isolates of Citrus tristeza virus for cross protection. AMB Express 2019, 9, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Morris, T.; Robertson, B.; Gallagher, M. Rapid reverse transcription-PCR detection of hepatitis C virus RNA in serum by using the TaqMan fluorogenic detection system. J. Clin. Microbiol. 1996, 34, 2933–2936. [Google Scholar] [CrossRef] [PubMed]
- Zhou, B.; Yang, G.; Hu, Z.; Chen, K.; Guo, W.; Wang, X.; Du, C. Development of a Real-Time Quantitative PCR Based on a TaqMan-MGB Probe for the Rapid Detection of Theileria haneyi. Microorganisms 2023, 11, 2633. [Google Scholar] [CrossRef]
- Vidal, E.; Yokomi, R.; Moreno, A.; Bertolini, E.; Cambra, M. Calculation of diagnostic parameters of advanced serological and molecular tissue-print methods for detection of Citrus tristeza virus: A model for other plant pathogens. Phytopathology 2012, 102, 114–121. [Google Scholar] [CrossRef]
- Lau, H.Y.; Botella, J.R. Advanced DNA-based point-of-care diagnostic methods for plant diseases detection. Front. Plant Sci. 2017, 8, 2016. [Google Scholar] [CrossRef]
- Osman, F.; Hodzic, E.; Kwon, S.J.; Wang, J.B.; Vidalakis, G. Development and validation of a multiplex reverse transcription quantitative PCR (RT-qPCR) assay for the rapid detection of Citrus tristeza virus, Citrus psorosis virus, and Citrus leaf blotch virus. J. Virol. Methods 2015, 220, 64–75. [Google Scholar] [CrossRef] [PubMed]
- Loconsole, G.; Saponari, M.; Savino, V. Development of real-time PCR based assays for simultaneous and improved detection of citrus viruses. Eur. J. Plant Pathol. 2010, 128, 251–259. [Google Scholar] [CrossRef]
- Yao, S.M.; Wu, M.L.; Hung, T.H. Development of Multiplex RT-PCR Assay for the Simultaneous Detection of Four Systemic Diseases Infecting Citrus. Agriculture 2023, 13, 1227. [Google Scholar] [CrossRef]
- Adkar-Purushothama, C.R.; Quaglino, F.; Casati, P.; Bianco, P.A. Reverse transcription-duplex-polymerase chain reaction for simultaneous detection of Citrus tristeza virus and ‘Candidatus Liberibacter’ from citrus plants. J. Plant Dis. Prot. 2010, 117, 241–243. [Google Scholar] [CrossRef]
- Saponari, M.; Loconsole, G.; Liao, H.H.; Jiang, B.; Savino, V.; Yokomi, R.K. Validation of high-throughput real time polymerase chain reaction assays for simultaneous detection of invasive citrus pathogens. J. Virol. Methods 2013, 193, 478–486. [Google Scholar] [CrossRef] [PubMed]
- Ananthakrishnan, G.; Venkataprasanna, T.; Roy, A.; Brlansky, R. Characterization of the mixture of genotypes of a Citrus tristeza virus isolate by reverse transcription-quantitative real-time PCR. J. Virol. Methods 2010, 164, 75–82. [Google Scholar] [CrossRef]
- Olmos, A.; Cambra, M.; Esteban, O.; Gorris, M.T.; Terrada, E. New device and method for capture, reverse transcription and nested PCR in a single closed-tube. Nucleic Acids Res. 1999, 27, 1564–1565. [Google Scholar] [CrossRef]
- Adkar-Purushothama, C.R.; Maheshwar, P.K.; Sano, T.; Janardhana, G.R. A Sensitive and Reliable RT-Nested PCR Assay for Detection of Citrus tristeza Virus from Naturally Infected Citrus Plants. Curr. Microbiol 2011, 62, 1455–1459. [Google Scholar] [CrossRef]
- Hindson, B.J.; Ness, K.D.; Masquelier, D.A.; Belgrader, P.; Heredia, N.J.; Makarewicz, A.J.; Bright, I.J.; Lucero, M.Y.; Hiddessen, A.L.; Legler, T.C. High-throughput droplet digital PCR system for absolute quantitation of DNA copy number. Anal. Chem. 2011, 83, 8604–8610. [Google Scholar] [CrossRef]
- Hayden, R.; Gu, Z.; Ingersoll, J.; Abdul-Ali, D.; Shi, L.; Pounds, S.; Caliendo, A. Comparison of droplet digital PCR to real-time PCR for quantitative detection of cytomegalovirus. J. Clin. Microbiol. 2013, 51, 540–546. [Google Scholar] [CrossRef]
- Taylor, S.C.; Laperriere, G.; Germain, H. Droplet Digital PCR versus qPCR for gene expression analysis with low abundant targets: From variable nonsense to publication quality data. Sci. Rep. 2017, 7, 2409. [Google Scholar] [CrossRef] [PubMed]
- Lei, S.; Chen, S.; Zhong, Q. Digital PCR for accurate quantification of pathogens: Principles, applications, challenges and future prospects. Int. J. Biol. Macromol. 2021, 184, 750–759. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.; Cui, L.; Wang, Y.; Xie, Z.; Wei, Y.; Zhu, S.; Nawaz, M.; Mak, W.-C.; Ho, H.-P.; Gu, D. An Integrated ddPCR Lab-on-a-Disc Device for Rapid Screening of Infectious Diseases. Biosensors 2023, 14, 2. [Google Scholar] [CrossRef] [PubMed]
- Ghosh, D.K.; Warghane, A.; Biswas, K.K. Rapid and Sensitive Detection of Citrus tristeza virus Using Reverse Transcription Loop-Mediated Isothermal Amplification (RT-LAMP) Assay. In Citrus Tristeza Virus: Methods and Protocols; Catara, A.F., Bar-Joseph, M., Licciardello, G., Eds.; Humana Press Inc.: Totowa, NJ, USA, 2019; Volume 2015, pp. 143–150. [Google Scholar] [CrossRef]
- Warghane, A.; Misra, P.; Bhose, S.; Biswas, K.K.; Sharma, A.K.; Reddy, M.K.; Ghosh, D.K. Development of a simple and rapid reverse transcription-loop mediated isothermal amplification (RT-LAMP) assay for sensitive detection of Citrus tristeza virus. J. Virol. Methods 2017, 250, 6–10. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, H.V.; Nguyen, V.D.; Liu, F.; Seo, T.S. An integrated smartphone-based genetic analyzer for qualitative and quantitative pathogen detection. ACS Omega 2020, 5, 22208–22214. [Google Scholar] [CrossRef] [PubMed]
- Chatzivassiliou, E.K.; Nolasco, G. Detection of a new variant of Citrus tristeza virus in Greek citrus crops. Phytopathol. Mediterr. 2014, 53, 140–147. [Google Scholar]
- Zhou, Y.; Zhou, C.; Liu, K.; Liu, Y.; Wang, X. Influence of the quantity and variability of citrus tristeza virus on transmissibility by single Toxoptera citricida. J. Plant Pathol. 2011, 93, 97–103. [Google Scholar]
- Morales, J.; Acosta, O.; Tamayo, P.; Peñaranda, J. Characterization of Citrus tristeza virus isolates from Colombia. Rev. De Protección Veg. 2013, 28, 45–53. [Google Scholar]
- Silva, G.; Fonseca, F.; Santos, C.; Nolasco, G. Presence of citrus tristeza virus in Angola and São Tomé e Príncipe: Characterization of isolates based on coat protein gene analysis. J. Plant Pathol 2007, 89, 149–152. [Google Scholar]
- Ferretti, L.; Fontana, A.; Sciarroni, R.; Schimio, R.; Loconsole, G. Molecular and biological evidence for a severe seedling yellows strain of Citrus tristeza virus spreading in southern Italy. Phytopathol. Mediterr. 2014, 53, 1–13. [Google Scholar]
- Oliveros-Garay, O.A.; Martinez-Salazar, N.; Torres-Ruiz, Y.; Acosta, O. CPm gene diversity in field isolates of Citrus tristeza virus from Colombia. Arch. Virol. 2009, 154, 1933–1937. [Google Scholar] [CrossRef] [PubMed]
- Davino, S.; Rubio, L.; Davino, M. Molecular analysis suggests that recent Citrus tristeza virus outbreaks in Italy were originated by at least two independent introductions. Eur. J. Plant Pathol. 2005, 111, 289–293. [Google Scholar] [CrossRef]
- Raspagliesi, D.; Licciardello, G.; Lombardo, G.; Catara, A.; Rizza, S. Quick characterization of Citrus tristeza virus isolates by capillary electrophoresis-single-strand conformation polymorphism. II Int. Symp. Citrus Biotechnol. 2009, 892, 183–188. [Google Scholar] [CrossRef]
- Chatzivassiliou, E.K.; Licciardello, G. Assessment of Genetic Variability of Citrus tristeza virus by SSCP and CE-SSCP. In Citrus Tristeza Virus: Methods and Protocols; Humana Press Inc.: Totowa, NJ, USA, 2019; pp. 79–104. [Google Scholar]
- Licciardello, G.; Russo, M.; Daden, M.; Bar-Joseph, M.; Catara, A.F. Capillary Electrophoresis-Single Strand Conformation Polymorphism Analysis and Multiple Molecular Marker Genotyping Allow a Rapid Differentiation of Citrus Tristeza Virus Isolates. Acta Hortic. 2015, 1065, 773–780. [Google Scholar] [CrossRef]
- Zanutto, C.A.; Corazza, M.J.; Nunes, W.M.d.C.; Müller, G.W. Evaluation of the protective capacity of new mild Citrus tristeza virus (CTV) isolates selected for a preimmunization program. Sci. Agric. 2013, 70, 116–124. [Google Scholar] [CrossRef]
- Licciardello, G.; Xiao, C.; Russo, M.; Dai, S.M.; Daden, M.; Deng, Z.N.; Catara, A.F. Genetic Structure of Citrus Tristeza Virus in Hunan Province (P.R. China). Acta Hortic. 2015, 1065, 781–790. [Google Scholar] [CrossRef]
- Mukhametzyanov, R.R.; Brusenko, S.V.; Khezhev, A.M.; Kelemetov, E.M.; Kirillova, S.S. Changing the Global Production and Trade of Citrus Fruits. In Sustainable Development of the Agrarian Economy Based on Digital Technologies and Smart Innovations; Springer: Cham, Switzerland, 2024; pp. 19–24. [Google Scholar]
- Černi, S.; Hančević, K.; Škorić, D. Citruses in Croatia–cultivation, major virus and viroid threats and challenges. Acta Bot. Croat. 2020, 79, 228–235. [Google Scholar] [CrossRef]
- Folimonova, S.Y. Developing an understanding of cross-protection by Citrus tristeza virus. Front. Microbiol. 2013, 4, 76. [Google Scholar] [CrossRef]
Type | Advantages | Limitations | Sample Type | Antibodies | Characteristics | References |
---|---|---|---|---|---|---|
ELISA | Commercially available Convenient for large volume detection High sensitivity and specificityLow cost | Sophisticated equipment is required Tedious procedure | Crude leaf sap | MCA13 MCAs, 3DF1 + 3CA5 MCAs | Multiantibody coating and monoclonal antibody were used as primary antibodies for detection | [23] |
DTBIA | Convenient for long time storage and long distance transportation Can be tested away from the lab Low cost | Subjective interpretation Sensitivity limitation | Pieces of membranes harboring the printed samples | 3DF1 + 3CA5 MCAs linked to AP or 3DF1 scFv-AP/S + 3CA5 scFvAP/S fusion proteins | No antibody coating required, pAbs, monoclonal antibodies or single chain antibodies are used | [41] |
LFIA | Easy to carry and use The detection time is short Result visualization Low cost | The sample needs to be pretreated into a liquid Sensitivity limitation | Crude leaf sap | Capture antibody (goat anti-CTV antibody) | Capture antibody was used for detection | [32] |
Immuno-electron microscopy (EM) | The virion morphology can be observed Lesions can be observed | Comparatively higher cost Difficult to detect high throughput | Tissue section/purified particles | 873, 894 and 879 pAbs | Polyclonal antibody was used for detection | [31] |
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Shang, P.; Xu, L.; Cheng, T. Serological and Molecular Detection of Citrus Tristeza Virus: A Review. Microorganisms 2024, 12, 1539. https://doi.org/10.3390/microorganisms12081539
Shang P, Xu L, Cheng T. Serological and Molecular Detection of Citrus Tristeza Virus: A Review. Microorganisms. 2024; 12(8):1539. https://doi.org/10.3390/microorganisms12081539
Chicago/Turabian StyleShang, Pengxiang, Longfa Xu, and Tong Cheng. 2024. "Serological and Molecular Detection of Citrus Tristeza Virus: A Review" Microorganisms 12, no. 8: 1539. https://doi.org/10.3390/microorganisms12081539