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Recent advances in Citrus psorosis virus

Abstract

Psorosis is a globally devastating disease of citrus caused by an infectious filamentous ophiovirus, Citrus psorosis virus (CPsV), which causes annual losses of about 5 % and a progressive decline of trees by affecting the conductive tissues. The disease can be harboured asymptomatically in many citrus species. In the field, the most characteristic symptoms of the disease in adult trees are bark scaling in the trunk and main branches and also internal staining in the underlying wood. The virus has a tripartite single-stranded RNA genome, and has been inadvertently spread to most citrus growing areas through the movement of citrus propagative material. No natural vectors have been identified except in limited citrus areas in some cases. Management strategies for CPsV involving shoot-tip grafting and thermotherapy or somatic embryogenesis from stigma and style cultures have been successfully used to eliminate CPsV from plant propagating material. Molecular pathogen-mediated strategies have been used to produce citrus plants. Such a strategy protects against infections by the virus from which the resistance gene and promising resistance may emerge from trials. Certification programs are among the best established means of increasing phytosanitary health, and some of those for citrus are among the oldest in the world. In conjunction with quarantine and clean stock programs, they remain important weapons in the ongoing fight against citrus diseases. One of the elements essential for successful certification programs to produce such propagation material is the availability of sensitive and effective diagnostic methods. In this review, we discuss an updated status of CPsV disease.

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References

  1. 1.

    Alioto D, Gangemi M, Deaglio S, Sposato S, Noris E, Luisoni E, Milne RG. Improved detection of Citrus psorosis virus using polyclonal and monoclonal antibodies. Plant Pathol. 1999;48:735–41.

    Article  Google Scholar 

  2. 2.

    Alioto D, Troisi A, Peluso A, Quatrano G, Masenga V, Milne RG. Occurence of Citrus psorosis virus in Campania, Southern Italy. Eur J Plant Pathol. 2000;106:795–9.

    Article  Google Scholar 

  3. 3.

    Alioto D, Malfitano M, Troisi A, Peluso A, Martín S, Milne RG, Guerri J, Moreno P. Variability of the coat protein gene of Citrus psorosis virus in Campania, southern Italy. Arch Virol. 2003;148:2155–66.

    CAS  PubMed  Article  Google Scholar 

  4. 4.

    Barragan-Valencia G, Morales-Loredo A, Alvarez-Ojeda MG, Rio MAPD, Quintero-Zapata I. Quantitative diagnosis of Citrus psorosis virus by real time RT-PCR. Agrociencia. 2008;42(2):225–32.

    Google Scholar 

  5. 5.

    Barthe GA, Ceccardi GL, Manjunath KL, Derrick KS. Citrus psorosis virus: nucleotide sequencing of the coat protein gene and detection by hybridization and RT-PCR. J Gen Virol. 1998;79:1531–7.

    CAS  PubMed  Google Scholar 

  6. 6.

    Carvalho SA, Santos FA, Machado MA. Psorosis virus complex elimination from citrus by shoot-tip-grafting associated to thermotherapy. Fitopatologia Brasileira. 2002;27(3):306–8.

    Article  Google Scholar 

  7. 7.

    Da Graça JV, Bar-Joseph M, Derrick KS. Inmunoblot detection of citrus psorosis in Israel using citrus ringspot antiserum. Proceedings of the 12th International Organisation of Citrus Virologists (IOCV) Conference, Riverside. 1993, pp 432–434.

  8. 8.

    Danos E. La psorosis de los cítricos: la epidemia en curso en Argentina y el desafio de su control. Revista de Investigaciones Agropecuarias. 1990;22:265–77.

    Google Scholar 

  9. 9.

    Derrick KS, Brlansky RH, da Graça JV, Lee RF, Timmer LW, Nguyen TK. Partial characterization of a virus associated with citrus ringspot. Phytopathology. 1988;78:1298–301.

    Article  Google Scholar 

  10. 10.

    Derrick KS, Lee RF, Hewitt BG, Barthe GA, da Graça JV. Characterization of citrus ringspot virus. In: Timmer LW, Garnsey SM, Navarro L, editors. Proceedings of the 11th International Organisation of Citrus Virologists (IOCV) Conference, Riverside. 1991, pp 386–390.

  11. 11.

    Djelouah K, Potere O, Boscia D, D’Onghia AM, Savino V. Production of monoclonal antibodies to citrus psorosis associated virus. In: da Graça JV, Lee RF, Yokomi RH, editors. Proceedings of the 14th International Organization of Citrus Virologists (IOCV) Conference, Riverside. 2000, pp 152–158.

  12. 12.

    D’Onghia AM, Djelouah K, Alioto KM, Castellano A, Savino V. Elisa correlates with biological indexing for the detection of Citrus psorosis virus associated virus. J Plant Pathol. 1998;80:157–63.

    Google Scholar 

  13. 13.

    D’Onghia AM, Djelouah K, Savino V. Serological detection of Citrus psorosis virus in seeds but not in seedlings of infected mandarin and sour orange. J Plant Pathol. 2000;82(3):233–5.

    Google Scholar 

  14. 14.

    D’Onghia AM, Carimi F, De Pasquale F, Djelouah K, Martelli GP. Elimination of Citrus psorosis virus by somatic embryogenesis from stigma and style cultures. Plant Pathol. 2001;50(2):266–9.

    Article  Google Scholar 

  15. 15.

    D’Onghia AM, Djelouah K, Frasheri D, Potere O. Detection of Citrus psorosis virus by direct tissue blot immunoassay. J Plant Pathol. 2001;83:139–42.

    Google Scholar 

  16. 16.

    EPPO. Data Sheets on Quarantine Pests: Citrus ringspot virus. Prepared by CABI and EPPO for the EU under Contract 90/399003. 2005. http://www.eppo.org/QUARANTINE/virus/Citrus_ringspot_virus/CIRSV0_ds.pdf.

  17. 17.

    Febres V, Fisher L, Khalaf A, Moore AG. Citrus transformation: challenges and prospects. Genetic transformation. 2011;101–22.

  18. 18.

    Garçia ML, Grau O, Sarachu AN. Citrus psorosis is probably caused by a bipartite ssRNA virus. Res Virol. 1991;142:303–11.

    PubMed  Article  Google Scholar 

  19. 19.

    Garçia ML, Dal Bó E, Grau O, Milne RG. The closely related citrus ringspot and Citrus psorosis viruses have particles of novel filamentous morphology. J Gen Virol. 1994;75:3585–90.

    PubMed  Article  Google Scholar 

  20. 20.

    Garçia ML, Sánchez de la Torre ME, Dal Bó E, Djelouah K, Luisoni E, Milne RG, Grau O. Detection of citrus psorosis-ringspot using RT-PCR and ELISA. Plant Pathol. 1997; 46:830–6.

  21. 21.

    Gottwald TR, Palle SR, Miao H, Seyran M, Skaria M, da Graça JV. Assessment of the possibility of natural spread of citrus psorosis disease. Proceedings of the 16th International Organization of Citrus Virologists (IOCV) Conference, Riverside. 2005, pp 240–250.

  22. 22.

    Kawazu Y, Sasaya T, Morikawa T, Sugiyama K, Natsuaki T. Nucleotide sequence of the coat protein gene of Mirafiori lettuce virus. J Gen Plant Pathol. 2003;69:55–60.

    CAS  Article  Google Scholar 

  23. 23.

    Kayim M, Barthe G, Beretta J, Derrick K. Transgenic citrus plants expressing the coat protein gene of Citrus psorosis virus. Phytopathology. 2005;95(6):S52–S52 Suppl.

    Google Scholar 

  24. 24.

    Khan IA. Citrus genetics, breeding and biotechnology. Cambridge: CABI Wallingford; 2007.

    Book  Google Scholar 

  25. 25.

    Lee RF, Lehmann P, Navarro L. Nursery practices, budwood and rootstock certification programs. In: Timmer LW, Duncan L, editors. Citrus health guide. St. Paul: APS Press Minn; 1999. p. 35–46.

    Google Scholar 

  26. 26.

    Legarreta GG, Garcia ML, Costa N, Grau O. A highly sensitive heminested RT-PCR assay for the detection of Citrus psorosis virus targeted to a conserved region of the genome. J Virol Methods. 2000;84:15–22.

    CAS  PubMed  Article  Google Scholar 

  27. 27.

    Loconsole G, Castellano MA, Dell’Orco M, Boscia D, Savino V. Serological detection of Citrus psorosis virus using a polyclonal antiserum to recombinant virus coat protein. J Plant Pathol. 2006;88:171–3.

    CAS  Google Scholar 

  28. 28.

    Loconsole G, Fatone MT, Savino V. Specific digoxigenin-labeled riboprobes for detection of Citrus prsorosis virus and Citrus variegation virus by molecular hybridization. J Plant Pathol. 2009;91(2):311–9.

    CAS  Google Scholar 

  29. 29.

    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;128:251–9.

    CAS  Article  Google Scholar 

  30. 30.

    Lot H, Campbell RN, Couche S, Milne RG, Roggero P. Transmisison by Olpidium brassicae of Mirafiori lettuce virus and Lettuce big-vein virus and their roles in lettuce big-vein etiology. Phytopathology. 2002;92:288–93.

    PubMed  Article  Google Scholar 

  31. 31.

    Luna GR, Peña EJ, Borniego MB, Heinlein M, Garcia ML. Ophioviruses CPsV and MiLBVV movement protein is encoded in RNA 2 and interacts with the coat protein. Virology. 2013;441(2):152–61.

    Article  Google Scholar 

  32. 32.

    Martín S, Alioto D, Milne RG, Guerri J, Moreno P. Detection of Citrus psorosis virus in field trees by direct tissue immunoassay in comparison with ELISA, symptomatology, biological indexing and cross-protection tests. Plant Pathol. 2002;51:134–41.

    Article  Google Scholar 

  33. 33.

    Martín S, Alioto D, Milne RG, Garnsey SM, García ML, Grau O. Detection of Citrus psorosis virus by ELISA, molecular hybridization, RT-PCR and immunosorbent electron microscopy and its association with citrus psorosis disease. Eur J Plant Pathol. 2004;110:747–57.

    Article  Google Scholar 

  34. 34.

    Martín S, López C, García ML, Naum-Onganía G, Grau O, Flores R. The complete nucleotide sequence of a Spanish isolate of Citrus psorosis virus: comparative analysis with other ophioviruses. Arch Virol. 2005;150(1):167–76.

    PubMed  Article  Google Scholar 

  35. 35.

    Martín S, García ML, Troisi A, Rubio L, Legarreta G, Grau O, Alioto D, Moreno P, Guerri J. Genetic variation of populations of Citrus psorosis virus. J Gen Virol. 2006;87:3097–102.

    PubMed  Article  Google Scholar 

  36. 36.

    Milne RG, Djelouah K, Garçia ML, Dal Bo E, Grau O. In: Structure of citrus-ringspot psorosis-associated virus particles: implication for diagnosis and taxonomy. Proceedings of the 13th International Organization of Citrus Virologists (IOCV) Conference, China. 1996, pp 189–97.

  37. 37.

    Milne RG, García ML, Moreno P. Citrus psorosis virus. In: AAB descriptions of plant viruses. 2003. No. 401.

  38. 38.

    Morikawa T, Nomura Y, Yamamoto T, Natsuaki T. Partial characterization of virus-like particles associated with Tulip mild mottle mosaic. Ann Phytopathol Soc Jpn. 1995;61:78–581.

    Article  Google Scholar 

  39. 39.

    Naum-Onganía G, Gago-Zachert S, Peña E, Grau O, García ML. Citrus psorosis virus RNA 1 is of negative polarity and potentially encodes in its complementary strand a 24K protein of unknown function and 280K putative RNA dependent RNA polymerase. Virus Res. 2003;96:49–61.

    PubMed  Article  Google Scholar 

  40. 40.

    Navarro JA, Torok VA, Vetten HJ, Pallas V. Genetic variability in the coat protein genes of Lettuce big-vein associated virus and Mirafiori lettuce big-vein virus. Arch Virol. 2005;150:681–94.

    CAS  PubMed  Article  Google Scholar 

  41. 41.

    Navarro L. Citrus sanitation, quarantine and certification programs. Moreno P, da Graça JV, Timmer LW, editors. Proceedings of the 12th International Organization of Citrus Virologists (IOCV) Conference, Riverside. 1993, pp 383–91.

  42. 42.

    Navas-Castillo J, Moreno P. Biological diversity of citrus ringspot isolates in Spain. Plant Pathol. 1993;42:347–57.

    Article  Google Scholar 

  43. 43.

    Navas-Castillo J, Moreno P. Filamentous flexuous particles and serologically related proteins of variable size associated with citrus psorosis and ringspot diseases. Eur J Plant Pathol. 1995;101:343–8.

    Article  Google Scholar 

  44. 44.

    Palle SR, Miao H, Seyran M, Louzada ES, da Graça JV, Skaria M. Evidence for association of Citrus psorosis virus with symptomatic trees and an Olpidium-like fungus. Proceedings of the 14th International Organisation of Citrus Virologists (IOCV) Conference, Riverside. 2005, pp 423–6.

  45. 45.

    Peña E, Luna GR, Zanek MC, Garçia ML. Citrus psorosis virus: insights into virus biology. Proceedings of the 18th International Organisation of Citrus Virologists (IOCV) Conference, Riverside. 2010, p 52.

  46. 46.

    Potere O, Boscia D, Djelouah K, Elicio V, Savino V. Use of monoclonal antibodies to Citrus psorosis virus for diagnosis. J Plant Pathol. 1999;81:209–12.

    CAS  Google Scholar 

  47. 47.

    Powell CA, Pelosi RR, Sodona RM. A psorosis like agent prevalent is Florida’s Grapefruit groves and budwood sources. Plant Dis. 1998;82(2):208–9.

    Article  Google Scholar 

  48. 48.

    Reyes CA, Peńa EJ, Zanek MC, Sanchez DV, Grau O, García ML. Differential resistance to Citrus psorosis virus in transgenic Nicotiana benthamiana plants expressing hairpin RNA derived from the coat protein and 54K protein genes. Plant Cell Rep. 2009;28:1817–25.

    CAS  PubMed  Article  Google Scholar 

  49. 49.

    Reyes CA, De Francesco A, Pena EJ, Costa N, Plata MI, Sendin L, Castagnaro AP, Garcia ML. Resistance to Citrus psorosis virus in transgenic sweet orange plants is triggered by coat protein-RNA silencing. J Biotech. 2011;151(1):151–8.

    CAS  Article  Google Scholar 

  50. 50.

    Reyes CA, Zanek MC, Velázquez K, Costa N, Plata MI, Garçia ML. Generation of sweet orange transgenic lines and evaluation of citrus psorosis virus-derived resistance against psorosis A and psorosis B. J Phytopathol. 2011;159:531–7.

    CAS  Article  Google Scholar 

  51. 51.

    Rochon D, Kakani K, Robbins M, Reade R. Molecular aspectes of plant virus transmission by Olpidium and Plasmodiophorid vectors. Annu Rev Phytopathol. 2004;42:211–41.

    CAS  PubMed  Article  Google Scholar 

  52. 52.

    Roggero P, Ciuffo M, Vaira AM, Accotto GP, Masenga V, Milne RG. An Ophiovirus isolated from lettuce with big-vein symptoms. Arch Virol. 2000;145:2629–42.

    CAS  PubMed  Article  Google Scholar 

  53. 53.

    Roistacher CN. Graft-transmissible diseases of citrus. Handbook for detection and diagnosis. Rome: Food and Agriculture Organization of the United Nations (FAO); 1991. p. 115–26.

    Google Scholar 

  54. 54.

    Roistacher CN. Psorosis-A Review. In: Moreno P, da Graça JV, Timmer LW, editors. Proceedings of the 12th International Organisation of Citrus Virologists (IOCV) Conference, Riverside. 1993, pp 139–54.

  55. 55.

    Rosa C, Polek M, Falk BW, Rowhani A. Improved efficiency for quantitative and qualitative indexing for Citrus tristeza virus and Citrus psorosis virus. Plant Dis. 2007;91:1089–95.

    CAS  Article  Google Scholar 

  56. 56.

    Rouag N, Kichi A, Lousini E, Melin R. Etude comparative des relations sérologiques, morphologiques et moléculaires entre le Citrus Ringspot et le Citrus psorosis virus. In: Rapport du 9ème Congrès Arabe pour la Protection des Végétaux, Damas, Syrie. 2006.

  57. 57.

    Roy A, Fayad A, Barthe G, Brlansky RH. A multiplex polymerase chain reaction method for reliable, sensitive and simultaneous detection of multiple viruses in citrus trees. J Virol Methods. 2005;129:47–55.

    CAS  PubMed  Article  Google Scholar 

  58. 58.

    Sánchez de la Torre ME, Riva O, Zandomeni R, Grau O, Garcia ML. The top component of Citrus psorosis virus contains two ssRNAs, the smaller encodes the coat protein. Mol Plant Pathol. 1998. http://www.bspp.org.uk/mppol/1998/1019sanchez.

  59. 59.

    Sánchez de la Torre ME, López C, Grau O, Garcia ML. RNA 2 of citrus psorosis virus is of negative polarity and contains a single open reading frame in its complementary strand. J Gen Virol. 2002;83:1777–81.

  60. 60.

    Sasaya T, Koganezawa H. Molecular analysis and virus transmission tests place Olpidium virulentus, a vector of Mirafiori lettuce big-vein virus and tobacco stunt virus, as a distinct species rather than a strain of Olpidium brassicae. J Gen Plant Pathol. 2006;72:20–5.

    CAS  Article  Google Scholar 

  61. 61.

    Skaria M, Miao H, Avila E. Post-freeze status of Citrus psorosis virus in Texas. Proceedings of the 15th International Organisation of Citrus Virologists (IOCV) Conference, Riverside. 2002, pp 366–7.

  62. 62.

    Sofy AR, Moussa AA, Fahmy H, Ghazal SA, El-Dougdoug KA. Anatomical and ultrastructural changes in Citrus leaves infected with Citrus psorosis virus Egyptian isolates. J Appl Sci Res. 2007;3(6):485–94.

    Google Scholar 

  63. 63.

    Torok VA and Vetten HJ. Characterization of an ophiovirus associated with lettuce ring necrosis. Joint Conference International Working Groups on Legume and Vegetable Viruses (Abstract), Bonn. 2002, p 4.

  64. 64.

    Torok VA and Vetten HJ. Identification and molecular characterization of a new ophiovirus associated with lettuce ring necrosis disease. Proceedings of Arbeitskreis Viruskrankheiten der Pflanzen, Heidelberg, Germany. 2003.

  65. 65.

    Torok VA, Vetten HI. Ophiovirus associated with lettuce ring necrosis (Abstract). Cernobbio: European Society for Virology Meeting; 2010. p. 282.

    Google Scholar 

  66. 66.

    Vaira AM, Milne RG, Accotto GP, Luisoni E, Masenga V, Lisa V. Partial characterization of a new virus from ranunculus with a divided RNA genome and circular supercoiled thread-like particles. Arch Virol. 1997;142:2131–46.

    CAS  PubMed  Article  Google Scholar 

  67. 67.

    Vaira AM, Accotto GP, Costantini A, Milne RG. The partial sequence of RNA1 of the ophiovirus Ranunculus white mottle virus indicates its relationship to rhabdovirus and provides candidate primers for an ophiovirus-specific RT-PCR test. Arch Virol. 2003;148:1037–50.

    CAS  PubMed  Article  Google Scholar 

  68. 68.

    Vaira AM, Lisa V, Costantini A, Masenga V, Rapetti S, Milne RG. Ophioviruses infecting ornamentals and a probable new species associated with a severe disease in freesia. Acta Hort. 2006;722:191–9.

    CAS  Google Scholar 

  69. 69.

    Vaira AM, Kleynhans R, Hammond J. First report of Freesia sneak virus infecting Lachenalia cultivars in South Africa. Plant Dis. 2007;91(6):770.

    Article  Google Scholar 

  70. 70.

    Vaira AM, Hammond J. An update on Freesia sneak virus, a new species in the Ophiovirus genus. 12th ISVDOP, Haarlem, The Netherlands. 2008.

  71. 71.

    Vaira AM, Milne RG. Ophiovirus. In: Mahy BWJ, Van Regenmortel M, editors. Encyclopedia of Virology. Oxford: Elsevier; 2008. p. 447–54.

    Chapter  Google Scholar 

  72. 72.

    Vaira AM, Hansen MA, Murphy C, Reinsel MD, Hammond J. First report of Freesia sneak virus in Freesia sp. in Virginia. Plant Dis. 2009;93(9):965.

    Article  Google Scholar 

  73. 73.

    Vaira AM, Gago-Zachert S, García ML, Guerri J, Hammond J, Milne RG, Moreno P, Morikawa T, Natsuaki T, Navarro JA, Pallás V, Torok V, Verbeek M, Vetten HJ. Ophioviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ, editors. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. 2011. p. 743–8.

  74. 74.

    Van der Wilk F, Dullemans AM, Verbeek M, van den Heuvel JM. Nucleotide sequence and genomic organization of an Ophiovirus associated with lettuce bug-vein disease. J Gen Virol. 2002;83:2869–77.

    PubMed  Google Scholar 

  75. 75.

    Vapnek J. Legislatively establishing a health certification programme for Citrus. FAO legal papers online. 2009. http://www.fao.org/lega/prs-o1/1po81.pdf.

  76. 76.

    Velázquez K, Renovell M, Comellas P, Serra M, García ML, Pina JA, Navarro L, Moreno P, Guerri J. Effect of temperature on RNA silencing of a negative stranded RNA plant virus: Citrus psorosis virus. Plant Pathol. 2010;59:982–90.

    Article  Google Scholar 

  77. 77.

    Velázquez K, Pina JA, Navarro L, Moreno P, Guerr J. Association of citrus psorosis B symptoms with a sequence variant of the Citrus psorosis virus RNA2. Plant Pathol. 2012;61:448–56.

    Article  Google Scholar 

  78. 78.

    Vidalakis G, da Graça JV, Dixon WN, Ferrin D, Kesinger M, Krueger RR, Lee RF, Melzer MJ, Olive J, Polek M, Sieburth PJ, Williams LL, Wright GC. Citrus Quarantine Sanitary and Certification Programs in the USA. Citrograph. 2010;3:26–35.

    Google Scholar 

  79. 79.

    Voinnet O. RNA silencing as a plant immune system against viruses. Trends Genet. 2001;17(8):499–500.

    Article  Google Scholar 

  80. 80.

    Zanek MC, Peña E, Reyes CA, Figueroa J, Stein B, Grau O, Garcia ML. Detection of Citrus psorosis virus in the northwestern citrus production area of Argentina by using an improved TAS-ELISA. J Virol Methods. 2006;137:245–51.

    CAS  PubMed  Article  Google Scholar 

  81. 81.

    Zanek MC, Reyes CA, Cervera M. Genetic transformation of sweet orange with the coat protein gene of Citrus psorosis virus and evaluation of resistance against the virus. Plant Cell Rep. 2008;27:57–66.

    CAS  PubMed  Article  Google Scholar 

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Achachi, A., Ait Barka, E. & Ibriz, M. Recent advances in Citrus psorosis virus . VirusDis. 25, 261–276 (2014). https://doi.org/10.1007/s13337-014-0199-7

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Keywords

  • Citrus psorosis virus
  • Ophiovirus
  • Segmented negative-stranded RNA virus
  • Diagnostics
  • Viral resistance
  • Certification