Papaya ringspot virus-P: Characteristics, pathogenicity, sequence variability and control

Molecular Plant Pathology

Volumn 9, Issue 3, 2008, Pages 269-280

  Tripathi, Savarni ^a   Suzuki, Jon Y ^a   Ferreira, Stephen A ^b   Gonsalves, Dennis ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b UNIVERSITY OF HAWAII AT MANOA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; COAT PROTEIN, PAPAYA RINGSPOT VIRUS; UNCLASSIFIED DRUG; VIRUS RNA;

CLASSIFICATION; GENETICS; METABOLISM; PAPAYA; PATHOGENICITY; PHYLOGENY; PLANT DISEASE; PLANT VIRUS; REVIEW; VIROLOGY; VIRULENCE; VIRUS GENOME;

CAPSID PROTEINS; CARICA; GENOME, VIRAL; PHYLOGENY; PLANT DISEASES; PLANT VIRUSES; RNA, VIRAL; VIRULENCE;

ACER PENSYLVANICUM; AMARANTHACEAE; APHIDIDAE; CARICA PAPAYA; CARICACEAE; CHENOPODIUM AMARANTICOLOR; CHENOPODIUM QUINOA; CUCUMIS; CUCUMIS METULIFERUS; CUCUMIS SATIVUS; CUCURBITA PEPO; CUCURBITACEAE; PAPAYA RINGSPOT VIRUS; PAPAYA RINGSPOT VIRUS P; POTYVIRIDAE; POTYVIRUS;

EID: 42249091348     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2008.00467.x     Document Type: Review

References (80)

1. Adams, M.J., Antoniw, J.F. Beaudoin, F. (2005) Review: overview and analysis of the polyprotein cleavage sites in the family Potyviridae. Mol. Plant Pathol. 6, 471 487.
2. An, G. (1986) Development of plant promoter expression vectors and their use for analysis of differential activity of nopaline synthase promoter in transformed tobacco cells. Plant Physiol. 81, 86 91.
3. An, G., Ebert, P.R., Mitra, A. Ha, S.B. (1988) Binary vectors. In : Plant Molecular Biology Manual (Gelvin, S. Schilperoort, R.A., eds pp. 1 19. Boston : Kluwer Academic Publishers.
4. Bateson, M., Henderson, J., Chaleeprom, W., Gibbs, A. Dale, J. (1994) Papaya ringspot potyvirus: isolate variability and origin of PRSV type P (Australia). J. Gen. Virol. 75, 3547 3553.
5. Bateson, M.F., Lines, R.E., Revill, P., Chaleeprom, W., Ha, C.V., Gibbs, A.J. Dale, J.L. (2002) On the evolution and molecular epidemiology of the potyvirus Papaya ringspot virus. J. Gen. Virol. 83, 2575 2585.
6. Bau, H.J., Cheng, Y.H., Yu, T.A., Yang, J.S., Liou, P.C., Hsiao, C.H., Lin, C.Y. Yeh, S.D. (2004a) Field evaluation of transgenic papaya lines carrying the coat protein gene of Papaya ringspot virus in Taiwan. Plant Dis. 85, 594 599.
7. Bau, H.J., Cheng, Y.H., Yu, T.A., Yang, J.S. Yeh, S.D. (2003) Broad-spectrum resistance to different geographic strains of Papaya ringspot virus in coat protein gene transgenic papaya. Phytopathology, 93, 112 120.
8. Bau, H.J., Tripathi, S., Chen, L.F., Cheng, Y.H., Yu, T.A., Yang, J.S. Yeh, S.D. (2004b) Transgenic papaya for control of papaya ringspot virus and analysis of viral factors involved in resistance breakdown. In : 10th SCBA International Symposium Vol. W-21-04. Beijing, China.
9. Chen, G., Ye, C.M., Huang, J.C., Yu, M. Li, B.J. (2001a) Cloning of the papaya ringspot virus (PRSV) replicase gene and generation of PRSV-resistant papayas through the introduction of the PRSV replicase gene. Plant Cell Rep. 20, 272 277.
10. Chen, K.C., Wang, C.H., Liu, F.L., Su, W.C. Yeh, S.D. (2001b) Construction of in vitro infectious clone of a type W strain of Papaya ringspot virus and analysis of host determinant for papaya infection. Plant Pathol. Bull. 10, 215 216.
11. Chen, K.C., Wang, C.H., Liu, F.L., Su, W.C. Yeh, S.D. (2003) The NIa gene of Papaya ringspot virus is the host determinant for papaya infection. In : 7th International Congress of Plant Molecular Biology. Barcelona, Spain.
12. Chen, L.F., Bau, H.J. Yeh, S.D. (2002) Identification of viruses capable of breaking transgenic resistance of papaya conferred by the coat protein gene of papaya ringspot virus. Acta Hortic. 575, 465 474.
13. Cheng, Y.H., Yang, J.S. Yeh, S.D. (1996) Efficient transformation of papaya by coat protein gene of papaya ringspot virus mediated by Agrobacterium following liquid-phase wounding of embryogenic tissues with carborundum. Plant Cell Rep. 16, 127 132.
14. Chiang, C.H., Lee, C.Y., Wang, C.H, Jan, F.J., Lin, S.S., Chen, T.C., Raja, J. Yeh, S.D. (2007) Genetic analysis of an attenuated Papaya ringspot virus strain applied for cross-protection. Eur. J. Plant Pathol. 118, 333 348.
15. Chiang, C.H., Wang, J.J., Jan, F.J., Yeh, S.D. Gonsalves, D. (2001) Comparative reactions of recombinant papaya ringspot viruses with chimeric coat protein (CP) genes and wild-type viruses on CP-transgenic papaya. J. Gen. Virol. 82, 2827 2836.
16. Chiang, C.H. Yeh, S.D. (1997) Infectivity assays of in vitro and in vivo transcripts of papaya ringspot potyvirus. Bot. Bull. Acad. Sinica, 38, 153 163.
17. Chin, M, Ahmad, M.H. Tennant, P. (2007) Momordica charantia is a weed host reservoir for Papaya ringspot virus type P in Jamaica. Plant Dis. 91, 1518.
18. Davis, M.J. Ying, Z. (2004) Development of papaya breeding lines with transgenic resistance to Papaya ringspot virus. Plant Dis. 88, 352 358.
19. Fermin, D. Gonsalves, D. (2003) Papaya: engineering resistance against papaya ringspot virus by native, chimeric and synthetic transgenes. In : Virus and Virus-like Diseases of Major Crops in Developing Countries (Loebenstein, G. Thottappilly, G., eds pp. 497 518. Dordrecht, The Netherlands : Kluwer Academic Publishers.
20. Fermin, G., Tennant, P., Gonsalves, C., Lee, D. Gonsalves, D. (2004) Comparative development and impact of transgenic papayas in Hawaii, Jamaica, and Venezuela. In : Transgenic Plants: Methods and Protocols (Pena, L., ed. pp. 399 430. Totowa, NJ : The Human Press Inc.
21. Ferreira, S.A., Mau, R.F.L., Manshardt, R., Pitz, K.Y. Gonsalves, D. (1992) Field evaluation of papaya ringspot virus cross protection. In : Proceedings of the 28th Annual Hawaii Papaya Industry Association Conference, pp. 14 19. Honolulu : USA.
22. Ferreira, S.A., Pitz, K.Y., Manshardt, R., Zee, F., Fitch, M. Gonsalves, D. (2002) Virus coat protein transgenic papaya provides practical control of papaya ringspot virus in Hawaii. Plant Dis. 86, 101 105.
23. Fitch, M.M.M., Manshardt, R.M., Gonsalves, D., Slightom, J.L. Sanford, J.C. (1990) Stable transformation of papaya via microprojectile bombardment. Plant Cell Rep. 9, 189 194.
24. Fitch, M.M.M., Manshardt, R.M., Gonsalves, D., Slightom, J.L. Sanford, J.C. (1992) Virus resistant papaya derived from tissues bombarded with the coat protein gene of papaya ringspot virus. Bio/Technology, 10, 1466 1472.
25. Fuchs, M. Gonsalves, G. (2007) Safety of virus-resistant transgenic plants two decades after their introduction: Lesson from realistic field risk assessment studies. Annu. Rev. Phytopathol. 47, 173 202.
26. Gonsalves, D. (1998) Control of papaya ringspot virus in papaya: a case study. Annu. Rev. Phytopathol. 36, 415 437.
27. Gonsalves, D. (2006) Transgenic papaya: development, release, impact, and challenges. Adv. Virus Res. 67, 317 354.
28. Gonsalves, D. Fermin, G. (2004) The use of transgenic papaya to control papaya ringspot virus in Hawaii and transfer of this technology to other countries. In : Handbook of Plant Biotechnology (Christau, P. Klee, H., eds pp. 1165 1182. London, UK : John Wiley & Sons.
29. Gonsalves, D. Ferreira, S. (2003) Transgenic papaya: a case for managing risks of papaya ringspot virus in Hawaii. Plant Health Progress doi:
30. Gonsalves, D., Ferreira, S.A., Suzuki, J.Y. Tripathi, S. (2007a) Papaya. In : A Compendium of Transgenic Crop Plants (Kole, C. Hall, T.C., eds). London : Blackwell Publishing (in press).
31. Gonsalves, D. Garnsey, S.M. (1989) Cross protection techniques for control of plant virus diseases in the tropics. Plant Dis. 73, 592 597.
32. Gonsalves, D., Gonsalves, C., Ferreira, S., Pitz, K., Fitch, M., Manshardt, R. Slightom, J. (2004b) Transgenic virus resistant papaya: from hope to reality for controlling papaya ringspot virus in Hawaii. APSnet Feature Story for July 2004. http://www.apsnet.org/online/feature/ringspot
33. Gonsalves, D. Ishii, M. (1980) Purification and serology of papaya ringspot virus. Phytopathology, 70, 1028 1032.
34. Gonsalves, C., Lee, D.R. Gonsalves, D. (2004a) Transgenic virus-resistant papaya: the Hawaiian 'Rainbow' was rapidly adopted by farmers and is of major importance in Hawaii today. APSnet feature story for August-September 2004. http://www.apsnet.org/online/feature/rainbow.
35. Gonsalves, D., Suzuki, J.Y., Tripathi, S. Ferreira, S.A. (2007b) Papaya ringspot virus (Potyviridae). In : Encyclopedia of Virology (Mahy, B.W.J. van Regenmortel, M.H.V., eds). Oxford : Elsevier Ltd (in press).
36. Gonsalves, D., Vegas, A., Prasartsee, V., Drew, R., Suzuki, J.Y. Tripathi, S. (2006) Developing papaya to control Papaya ringspot virus by transgenic resistance, intergeneric hybridization, and tolerance breeding. In : Plant Breeding Reviews Vol. 26 (Janick, J., ed. pp. 35 73. Hoboken, NJ : John Wiley and Sons, Inc.
37. Ishii, M. Holtzmann, O.V. (1963) Papaya mosaic disease in Hawaii. Plant Dis. Rep. 47, 947 951.
38. Jain, R.K., Sharma, J., Sivakumar, A.S., Sharma, P.K., Byadgi, A.S., Verma, A.K. Varma, A. (2004) Variability in the coat protein gene of Papaya ringspot virus isolates from multiple locations in India. Arch. Virol. 149, 2435 2442.
39. Jensen, D.D. (1949) Papaya virus diseases with special reference to papaya ringspot. Phytopathology, 39, 191 211.
40. Lee, C.Y., Chiang, C.H. Yeh, S.D. (2001) Analyses of the roles of P1 and HC-Pro genes of Papaya ringspot virus for the attenuated symptoms on papaya plants and local lesion formation on Chenoposium quinoa. Plant Pathol. Bull. 10, 211 212.
41. Lines, R.E., Persley, D., Dale, J.L., Drew, R. Bateson, M.F. (2002) Genetically engineered immunity to Papaya ringspot virus in Australian papaya cultivars. Mol. Breeding, 10, 119 129.
42. Ling, K., Namba, S., Gonsalves, C., Slightom, J.L. Gonsalves, D. (1991) Protection against detrimental effects of potyvirus infection in transgenic tobacco plants expressing the papaya ringspot virus coat protein gene. Bio/Technology, 9, 752 758.
43. Lius, S., Manshardt, R.M., Fitch, M.M.M., Slightom, J.L., Sanford, J.C. Gonsalves, D. (1997) Pathogen-derived resistance provides papaya with effective protection against papaya ringspot virus. Mol. Breeding, 3, 161 168.
44. Maia, I.G., Haenni, A.L. Bernardi, F. (1996) Potyviral HC-Pro: a multifunctional protein. J. Gen. Virol. 77, 1335 1341.
45. Manshardt, R.M. (1992) Papaya. In : Biotechnology of Perennial Fruit Crops, Vol. 21 (Hammerschlag, F.A. Litz, R.E., eds pp. 489 511. Wallingford, UK : CAB International.
46. Manshardt, R.M. (1998) 'UH Rainbow' papaya. Univ. Hawaii Coll. Trop. Agric. Hum. Resources, New Plant for Hawaii-1, 2.
47. Manshardt, R.M. Wenslaff, T.F. (1989) Interspecific hybridization of papaya with other Carica species. J. Am. Soc. Hortic. Sci. 114, 689 694.
48. Mau, R.F.L., Gonsalves, D. Bautista, R. (1989) Use of cross protection to control papaya ringspot virus at Waianae. In : Proc. 25th Annu. Hawaii Papaya Ind. Assoc. Conf., pp. 77 84. Hawaii, USA.
49. Parris, G.K. (1938) A new disease of papaya in Hawaii. Proc. Am. Soc. Hortic. Sci. 36, 263 265.
50. Peng, Y.H., Kadoury, D., Gal-On, A., Huet, H., Wang, Y. Raccah, B. (1998) Mutations in the HC-Pro gene of zucchini yellow mosaic potyvirus: effects on aphid transmission and binding to purified virions. J. Gen. Virol. 79, 897 904.
51. Pirone, T.P. (1991) Viral genes and gene products that determine insect transmissibility. Semin. Virol. 2, 81 87.
52. Pirone, T.P. Blanc, S. (1996) Helper-dependent vector transmission of plant viruses. Annu. Rev. Phytopathol. 34, 227 247.
53. Pitz, K., Ferreira, S., Mau, R. Gonsalves, D. (1994) Papaya cross protection: the near-commercialization experience on Oahu. In : Proc. 30th Annu. Hawaii Papaya Ind. Assoc. Conf., pp. 4 6. Maui, USA.
54. Purcifull, D., Edwardson, J., Hiebert, E. Gonsalves, D. (1984) Papaya ringspot virus. CMI/AAB Descr. Plant Viruses, No. 209. (No. 84 Revis., July 1984), 8.
55. Quemada, H.D., Gonsalves, D. Slightom, J.L. (1991) Expression of coat protein gene from cucumber mosaic virus strain C in tobacco: protection against infections by CMV strains transmitted mechanically or by aphids. Phytopathology, 81, 794 802.
56. Quemada, H., L'Hostis, B., Gonsalves, D., Reardon, I.M., Heinrikson, R., Hiebert, E.L., Sieu, L.C. Slightom, J.L. (1990) The nucleotide sequences of the 3′-terminal regions of papaya ringspot virus strains w and p. J. Gen. Virol. 71, 203 210.
57. Ratcliff, F.G., MacFarlane, S.A. Baulcombe, D.C. (1999) Gene silencing without DNA: RNA-mediated cross-protection between viruses. Plant Cell, 11, 1207 1216.
58. Riechmann, J.L., Lain, S. Garcia, J.A. (1992) Highlights and prospects of potyvirus molecular biology. J. Gen. Virol. 73, 1 16.
59. Ruanjan, P., Kertbundit, S. Juricek, M. (2007) Post-transcriptional gene silencing is involved in resistance of transgenic papayas to papaya ringspot virus. Biol. Plantarum, 51, 517 520.
60. Sanford, J.C. Johnston, S.A. (1985) The concept of parasite-derived resistance - Deriving resistance genes from the parasite's own genome. J. Theor. Biol. 113, 395 405.
61. Silva-Rosales, L., Becerra-Leor, N., Ruiz-Castro, S., Teliz-Ortiz, D. Noa-Carrazana, J.C. (2000) Coat protein sequence comparisons of three Mexican isolates of papaya ringspot virus with other geographical isolates reveal a close relationship to American and Australian isolates. Arch. Virol. 145, 835 843.
62. Souza, M.T., Jr., Tennant, P.F. Gonsalves, D. (2005) Influence of coat protein transgene copy number on resistance in transgenic line 63-1 against Papaya ringspot virus isolates. HortScience, 40, 2083 2087.
63. Suzuki, J.Y., Tripathi, S. Gonsalves, D. (2007) Virus-resistant transgenic papaya: commercial development and regulatory and environmental issues. In : Biotechnology and Plant Disease Management (Punja, Z.K., DeBoer, S. Sanfacon, H., eds 336 361. Willingford, UK : CAB International.
64. Tennant, P., Fermin, G., Fitch, M.M., Manshardt, R.M., Slightom, J.L. Gonsalves, D. (2001) Papaya ringspot virus resistance of transgenic Rainbow and SunUp is affected by gene dosage, plant development, and coat protein homology. Eur. J. Plant Pathol. 107, 645 653.
65. Tennant, P.F., Gonsalves, C., Ling, K.S., Fitch, M., Manshardt, R., Slightom, J.L. Gonsalves, D. (1994) Differential protection against papaya ringspot virus isolates in coat protein gene transgenic papaya and classically cross-protected papaya. Phytopathology, 84, 1359 1366.
66. Tennant, P., Souza, M.T., Jr., Gonsalves, D., Fitch, M.M., Manshardt, R.M. Slightom, J.L. (2005) Line 63-1: a new virus-resistant transgenic papaya. HortScience, 40, 1196 1199.
67. Tripathi, S., Bau, H.J., Chen, L.F. Yeh, S.D. (2004) The ability of Papaya ringspot virus strains overcoming the transgenic resistance of papaya conferred by the coat protein gene is not correlated with higher degrees of sequence divergence from the transgene. Eur. J. Plant Pathol. 110, 871 882.
68. Tripathi, S., Chen, L.F., Bau, H.J. Yeh, S.D. (2003) In addition to transgene divergence potyviral HC-Pro gene plays an important role in breaking down coat protein gene-mediated transgene resistance. In : 7th International Congress of Plant Molecular Biology, p. 367.
69. Tripathi, S., Suzuki, J. Gonsalves, D. (2006) Development of genetically engineered resistant papaya for Papaya ringspot virus in a timely manner - A comprehensive and successful approach. In : Plant-Pathogen Interactions: Methods and Protocols Vol. 354 (Ronald, P., ed. pp. 197 240. Totowa, NJ : The Humana Press, Inc.
70. Wang, C.H. Yeh, S.D. (1997) Divergence and conservation of the genomic RNAs of Taiwan and Hawaii strains of papaya ringspot potyvirus. Arch. Virol. 142, 271 285.
71. Wang, H.L., Yeh, S.-D., Chiu, R.J. Gonsalves, D. (1987) Effectiveness of cross-protection by mild mutants of papaya ringspot virus for control of ringspot disease of papaya in Taiwan. Plant Dis. 71, 491 497.
72. Yeh, S.D. Gonsalves, D. (1984) Evaluation of induced mutants of papaya ringspot virus for control by cross protection. Phytopathology, 74, 1086 1091.
73. Yeh, S.D. Gonsalves, D. (1985) Translation of Papaya ringspot virus RNA in vitro: detection of a possible polyprotein that is processed for capsid protein, cylindrical-inclusion protein, and amorphous-inclusion protein. Virology, 143, 260 271.
74. Yeh, S.D. Gonsalves, D. (1994) Practices and perspective of control of papaya ringspot virus by cross protection. In : Advances in Disease Vector Research Vol. 10 (Harris, K.F., ed. pp. 237 257. New York : Springer.
75. Yeh, S.D., Gonsalves, D. Provvidenti, R. (1984) Comparative studies on host range and serology of papaya ringspot virus and watermelon mosaic virus 1. Phytopathology, 74, 1081 1085.
76. Yeh, S.D., Gonsalves, D., Wang, H.L., Namba, R. Chiu, R.J. (1988) Control of papaya ringspot virus by cross protection. Plant Dis. 72, 375 380.
77. Yeh, S.D., Jan, F.J., Chiang, C.H., Doong, P.J., Chen, M.C., Chung, P.H. Bau, H.J. (1992) Complete nucleotide sequence and genetic organization of papaya ringspot virus RNA. J. Gen. Virol. 73, 2531 2541.
78. Yeh, S.D., Tripathi, S., Bau, H.J. Chen, L.F. (2003) Identification and variability analyses of virus strains capable of breaking transgenic resistance of papaya conferred by the coat protein gene of Papaya ringspot virus. In : Abstracts 7th International Congress of Plant Molecular Biology, p. 367. Barcelona, Spain.
79. Yeh, S.D., You, B.J., Tripathi, S., Chen, L.F. Bau, H.J. (2005) Transgenic resistance overcome by potyviral Hc-Pro gene in a transgene sequence-homology independent manner. In : Microbes in Changing World. San Francisco, USA : International Union of Microbiological Societies.
80. You, B.J., Chiang, C.H., Chen, L.F., Su, W.C. Yeh, S.D. (2005) Engineered mild strain of Papaya ringspot virus for broader cross protection in cucurbits. Phytopathology, 95, 533 540.