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The Scientific World Journal
Volume 2014 (2014), Article ID 768038, 11 pages
http://dx.doi.org/10.1155/2014/768038
Review Article

Gene Technology for Papaya Ringspot Virus Disease Management

1Centre for General Studies, Universiti Kebangsaan Malaysia (UKM), 43600 Bangi, Selangor, Malaysia
2Department of Agricultural Extension, Khamarbari, Farmgate, Dhaka 1215, Bangladesh
3Faculty of Science and Technology, Universiti Kebangsaan Malaysia (UKM), 43600 Bangi, Selangor, Malaysia

Received 19 December 2013; Accepted 1 February 2014; Published 17 March 2014

Academic Editors: R. Dinkins and S. Rodtong

Copyright © 2014 Md. Abul Kalam Azad et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. DeCandolle, Origin of Cultivated Plants, John Wiley & Sons, New York, NY, USA, 1984.
  2. R. Jayavalli, T. N. Balamohan, N. Manivannan, and M. Govindaraj, “Breaking the intergeneric hybridization barrier in Carica papaya and Vasconcellea cauliflora,” Scientia Horticulturae, vol. 130, no. 4, pp. 787–794, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. M. A. K. Azad, M. G. Rabbani, and L. Amin, “Plant regeneration and somatic embryogenesis from immature embryos derived through interspecific hybridization among different Carica species,” International Journal of Molecular Science, vol. 13, pp. 17065–17076, 2012. View at Publisher · View at Google Scholar
  4. G. Aravind, D. Bhowmik, S. Duraivel, and G. Harish, “Traditional and medicinal uses of Carica papaya,” Journal of Medicinal Plants Studies, vol. 1, no. 1, pp. 7–15, 2013. View at Google Scholar
  5. A. M. O. Retuta, P. M. Magdalita, E. T. Aspuria, and R. R. C. Espino, “Evaluation of selected transgenic papaya (Carica papaya L) lines for inheritance of resistance to papaya ringspot virus and horticultural traits,” Plant Biotechnology, vol. 29, pp. 339–349, 2012. View at Publisher · View at Google Scholar
  6. S. D. Yeh and D. Gonsalves, “Evaluation of induced mutants of papaya ringspot virus for control by cross protection,” Phytopathology, vol. 74, pp. 1086–1091, 1984. View at Publisher · View at Google Scholar
  7. D. Gonsalves, “Control of papaya ringspot virus in papaya: a case study,” Annual Review of Phytopathology, vol. 36, pp. 415–437, 1998. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Tripathi, J. Y. Suzuki, S. A. Ferreira, and D. Gonsalves, “Papaya ringspot virus-P: characteristics, pathogenicity, sequence variability and control,” Molecular Plant Pathology, vol. 9, no. 3, pp. 269–280, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. D. E. Purcifull, J. R. Edwardson, E. Hiebert, and D. Gonsalves, “Papaya ringspot virus,” in CMI/AAB Description of Plant Viruses, R. E. Coronel, Ed., vol. 292, no. 2, p. 8, Wageningen University, Wageningen, The Netherlands, 1984. View at Google Scholar
  10. S. M. P. Khurana, “Studies on three virus diseases of papaya in Gorakhpur, India,” in Proceedings 19th International Horticulture Congress, vol. 7, p. 260, Warszawa, Poland, 1974.
  11. D. Gonsalves, “Papaya ringspot virus,” in Compendium of Tropical Fruit Diseases, R. C. Ploetz, G. A. Zentmyer, W. T. Nishijima, K. G. Rohrbach, and H. D. Ohr, Eds., pp. 67–68, APS Press, St. Paul, Minn, USA, 1994. View at Google Scholar
  12. H. F. Alvizo and C. Rojkind, “Resistencia al virus mancha anular del papayo en Carica cauliflora,” in Revista Mexicana De Fitopatología, vol. 5, pp. 61–62, 1987. View at Google Scholar
  13. J. E. Thomas and R. L. Dodman, “The first record of papaya ringspot virus-p in Australia,” Australian Plant Pathology, vol. 22, pp. 2–7, 1993. View at Publisher · View at Google Scholar
  14. T. Maoka, S. Kawano, and T. Usugi, “Occurrence of the P strain of papaya ringspot virus in Japan,” Annals of the Phytopathological Society, vol. 61, pp. 34–37, 1995. View at Publisher · View at Google Scholar
  15. R. I. Davis, L. Mu, N. Maireroa et al., “First records of the papaya strain of Papaya ringspot virus (PRSV-P) in French Polynesia and the Cook Islands,” Australasian Plant Pathology, vol. 34, no. 1, pp. 125–126, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. P. F. Tennant, G. A. Fermin, and R. E. Roye, “Viruses infecting papaya (Carica papaya L.): etiology, pathogenesis, and molecular biology,” Plant Viruses, vol. 1, pp. 178–188, 2007. View at Google Scholar
  17. I. G. Maia, A.-L. Haenni, and F. Bernardi, “Potyviral HC-Pro: a multifunctional protein,” Journal of General Virology, vol. 77, no. 7, pp. 1335–1341, 1996. View at Google Scholar · View at Scopus
  18. Y.-H. Peng, D. Kadoury, A. Gal-On, H. Huet, Y. Wang, and B. Raccah, “Mutations in the HC-Pro gene of zucchini yellow mosaic potyvirus: effects on aphid transmission and binding to purified virions,” Journal of General Virology, vol. 79, no. 4, pp. 897–904, 1998. View at Google Scholar · View at Scopus
  19. T. P. Pirone and S. Blanc, “Helper-dependent vector transmission of plant viruses,” Annual Review of Phytopathology, vol. 34, pp. 227–247, 1996. View at Publisher · View at Google Scholar · View at Scopus
  20. G. A. Fermin, L. T. Castro, and P. F. Tennant, “CP-transgenic and non-transgenic approaches for the control of papaya ringspot: current situation and challenges,” Transgenic Plant Journal, vol. 4, no. S1, pp. 1–15, 2010. View at Google Scholar
  21. J. A. Teixeira da Silva, Z. Rashid, D. T. Nut, and et. al, “Papaya (Carica papaya L.) biology and biotechnology,” Tree and Forestry Science and Biotechnology, vol. 1, pp. 47–73, 2007. View at Google Scholar
  22. S. Horovitz and H. Jimenez, “Cruzamientos interspecificos y intergenericos in Carica ceas y sus implicaciones fitotecnicas,” Agronomia Tropical (Maracay), vol. 17, pp. 323–343, 1967 (Spanish). View at Google Scholar
  23. M. Fuchs and D. Gonsalves, “Safety of virus-resistant transgenic plants two decades after their introduction: lessons from realistic field risk assessment studies,” Annual Review of Phytopathology, vol. 45, pp. 173–202, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. D. C. Baulcombe, “RNA as a target and an initiator of post-transcriptional gene silencing in trangenic plants,” Plant Molecular Biology, vol. 32, no. 1-2, pp. 79–88, 1996. View at Google Scholar · View at Scopus
  25. D. Gonsalves, S. Tripathi, J. B. Carr, and J. Y. Suzuki, “Papaya ringspot virus,” The Plant Health Instructor, 2010. View at Publisher · View at Google Scholar
  26. E. M. Tecson Mendoza, A. C. Laurena, and J. R. Botella, “Recent advances in the development of transgenic papaya technology,” Biotechnology Annual Review, vol. 14, pp. 423–462, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. S.-D. Yeh and D. Gonsalves, “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, vol. 143, no. 1, pp. 260–271, 1985. View at Google Scholar · View at Scopus
  28. S. Urcuqui-Inchima, A.-L. Haenni, and F. Bernardi, “Potyvirus proteins: a wealth of functions,” Virus Research, vol. 74, no. 1-2, pp. 157–175, 2001. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Anandalakshmi, G. J. Pruss, X. Ge et al., “A viral suppressor of gene silencing in plants,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 22, pp. 13079–13084, 1998. View at Publisher · View at Google Scholar · View at Scopus
  30. K. D. Kasschau and J. C. Carrington, “Long-distance movement and replication maintenance functions correlate with silencing suppression activity of potyviral HC-Pro,” Virology, vol. 285, no. 1, pp. 71–81, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. G. Pruss, X. Ge, X. M. Shi, J. C. Carrington, and V. B. Vance, “Plant viral synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses,” Plant Cell, vol. 9, no. 6, pp. 859–868, 1997. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Fernandez, S. Lain, and J. A. Garcia, “RNA helicase activity of the plum pox potyvirus CI protein expressed in Escherichia coli. Mapping of an RNA binding domain,” Nucleic Acids Research, vol. 23, no. 8, pp. 1327–1332, 1995. View at Google Scholar · View at Scopus
  33. S. Lain, J. L. Riechmann, and J. A. Garcia, “RNA helicase: a novel activity associated with a protein encoded by a positive strand RNA virus,” Nucleic Acids Research, vol. 18, no. 23, pp. 7003–7006, 1990. View at Google Scholar · View at Scopus
  34. P. F. Tennant, C. Gonsalves, K. S. Ling et al., “Differential protection against papaya ringspot virus isolates in coat protein gene transgenic papaya and classically cross-protected Papaya,” Phytopathology, vol. 84, no. 11, pp. 1359–1366, 1994. View at Google Scholar · View at Scopus
  35. M. F. Bateson, J. Henderson, W. Chaleeprom, A. J. Gibbs, and J. L. Dale, “Papaya ringspot potyvirus: isolate variability and the origin of PRSV type P (Australia),” Journal of General Virology, vol. 75, no. 12, pp. 3547–3553, 1994. View at Google Scholar · View at Scopus
  36. H. Quemada, B. L'Hostis, D. Gonsalves et al., “The nucleotide sequences of the 3'-terminal regions of papaya ringspot virus strains W and P,” Journal of General Virology, vol. 71, no. 1, pp. 203–210, 1990. View at Google Scholar · View at Scopus
  37. R. K. Jain, J. Sharma, A. S. Sivakumar et al., “Variability in the coat protein gene of Papaya ringspot virus isolates from multiple locations in India,” Archives of Virology, vol. 149, no. 12, pp. 2435–2442, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Silva-Rosales, N. Becerra-Leor, S. Ruiz-Castro, D. Téliz-Ortiz, and J. C. Noa-Carrazana, “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,” Archives of Virology, vol. 145, no. 4, pp. 835–843, 2000. View at Google Scholar · View at Scopus
  39. M. F. Bateson, R. E. Lines, P. Revill et al., “On the evolution and molecular epidemiology of the potyvirus Papaya ringspot virus,” Journal of General Virology, vol. 83, no. 10, pp. 2575–2585, 2002. View at Google Scholar · View at Scopus
  40. X. A. Olarte Castillo, G. Fermin, J. Tabima et al., “Phylogeography and molecular epidemiology of Papaya ringspot virus,” Virus Research, vol. 159, no. 2, pp. 132–140, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. D. Gonsalves and M. Ishii, “Purification and serology of papaya ringspot virus,” Phytopathology, vol. 70, no. 11, pp. 1028–1032, 1980. View at Publisher · View at Google Scholar
  42. G. Chen, C. M. Ye, J. C. Huang, M. Yu, and B. J. Li, “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 Reports, vol. 20, no. 3, pp. 272–277, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. C.-H. Chiang, C.-Y. Lee, C.-H. Wang et al., “Genetic analysis of an attenuated Papaya ringspot virus strain applied for cross-protection,” European Journal of Plant Pathology, vol. 118, no. 4, pp. 333–348, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. C. H. Wang, H. J. Bau, and S. D. Yeh, “Comparison of the nuclear inclusion b protein and coat protein genes of five papaya ringspot virus strains distinct in geographic origin and pathogenicity,” Phytopathology, vol. 84, no. 10, pp. 1205–1210, 1994. View at Google Scholar · View at Scopus
  45. S. D. Yeh, H. J. Bau, Y. H. Cheng, T. A. Yu, J. S. Yang, and R. A. Drew, “Greenhouse and field evaluations of coat-protein transgenic papaya resistant to papaya ringspot virus,” Acta Horticulturae, vol. 461, pp. 321–328, 1998. View at Google Scholar
  46. M. Sreenivasulu and D. V. R. SaiGopal, “Development of recombinant coat protein antibody based IC-RT-PCR and comparison of its sensitivity with other immunoassays for the detection of papaya ringspot virus isolates from India,” Plant Pathology Journal, vol. 26, no. 1, pp. 25–31, 2010. View at Google Scholar
  47. S. Ruiz-Castro and L. Silva-Rosales, “Use of RT-PCR for papaya ringspot virus detection in papaya (Carica papaya) plants from Veracruz, Tabasco and Chiapas,” Revista Mexicana de Fitopatologia, vol. 15, no. 1, pp. 83–87, 1997. View at Google Scholar
  48. F. D. Smith and E. E. Bantari, “Dot ELISA on nitrocellulose membrane for detection of potato leaf roll virus,” Plant Disease, vol. 71, pp. 795–799, 1987. View at Publisher · View at Google Scholar
  49. K. Pernezny and R. E. Litz, “Some common diseases of papaya in Florida,” Florida Cooperative Extension Service Plant Pathology Fact Sheet, p. 35, 1999.
  50. S. Dillon, C. Ramage, S. Ashmore, and R. A. Drew, “Development of a codominant CAPS marker linked to PRSV-P resistance in highland papaya,” Theoretical and Applied Genetics, vol. 113, no. 6, pp. 1159–1169, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. D. Gonsalves, A. Vegas, V. Prasartsee, R. A. Drew, J. Y. Suzuki, and S. Tripathi, “Developing papaya to control Papaya ringspot virus by transgenic resistance, intergeneric hybridization, and tolerance breeding,” in Plant Breeding Reviews, J. Janick, Ed., vol. 26, pp. 35–73, John Wiley & Sons, Hoboken, NJ, USA, 2006. View at Google Scholar
  52. R. M. Manshardt, “Papaya,” in Biotechnology of Perennial Fruit Crops, F. A. Hammerschlag and R. E. Litz, Eds., pp. 489–511, Cambridge University Press, Oxford, UK, 1992. View at Google Scholar
  53. D. Gonsalves and S. M. Garnsey, “Cross protection techniques for control of plant virus diseases in the tropics,” Plant Disease, vol. 73, no. 7, pp. 592–597, 1989. View at Google Scholar
  54. S. D. Yeh, D. Gonsalves, H. L. Wang et al., “Control of papaya ringspot virus by cross protection,” Plant Disease, vol. 22, pp. 375–380, 1988. View at Google Scholar
  55. S. D. Yeh and Y. H. Cheng, “Use of resistant Cucumis metuliferus for selection of nitrous-acid induced attenuated strains of papaya ringspot virus,” Phytopathology, vol. 79, no. 11, pp. 1257–1261, 1989. View at Publisher · View at Google Scholar
  56. J. C. Sanford and S. A. Johnston, “The concept of parasite-derived resistance: deriving resistance genes from the parasite's own genome,” Journal of Theoretical Biology, vol. 113, no. 2, pp. 395–405, 1985. View at Google Scholar · View at Scopus
  57. C.-H. Chiang, J.-J. Wang, F.-J. Jan, S.-D. Yeh, and D. Gonsalves, “Comparative reactions of recombinant papaya ringspot viruses with chimeric coat protein (CP) genes and wild-type viruses on CP-transgenic papaya,” Journal of General Virology, vol. 82, no. 11, pp. 2827–2836, 2001. View at Google Scholar · View at Scopus
  58. H.-J. Bau, Y.-H. Cheng, T.-A. Yu, J.-S. Yang, and S.-D. Yeh, “Broad-spectrum resistance to different geographic strains of Papaya ringspot virus in coat protein gene transgenic papaya,” Phytopathology, vol. 93, no. 1, pp. 112–120, 2003. View at Google Scholar · View at Scopus
  59. M. M. M. Fitch, R. M. Manshardt, D. Gonsalves, J. L. Slightom, and J. C. Sanford, “Virus resistant papaya plants derived from tissues bombarded with the coat protein gene of papaya ringspot virus,” Nature Biotechnology, vol. 10, no. 11, pp. 1466–1472, 1992. View at Publisher · View at Google Scholar · View at Scopus
  60. Y.-H. Cheng, J.-S. Yang, and S.-D. Yen, “Efficient transformation of papaya by coat protein gene of papaya ringspot virus mediated by Agrobacterium following liquid-phase wounding of embryogenic tissues with caborundum,” Plant Cell Reports, vol. 16, no. 3-4, pp. 127–132, 1996. View at Publisher · View at Google Scholar · View at Scopus
  61. R. E. Lines, D. Persley, J. L. Dale, R. Drew, and M. F. Bateson, “Genetically engineered immunity to Papaya ringspot virus in Australian papaya cultivars,” Molecular Breeding, vol. 10, no. 3, pp. 119–129, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. P. Tennant, M. H. Ahmad, and D. Gonsalves, “Transformation of Carica papaya L. with virus coat protein genes for studies on resistance to Papaya ringspot virus from Jamaica,” Tropical Agriculture, vol. 79, no. 2, pp. 105–113, 2002. View at Google Scholar · View at Scopus
  63. M. A. K. Azad, M. G. Rabbani, L. Amin, and N. M. Sidik, “Development of transgenic papaya through Agrobacterium mediated transformation,” International Journal of Genomics, vol. 2013, Article ID 235487, 5 pages, 2013. View at Publisher · View at Google Scholar
  64. M. J. Davis and Z. Ying, “Genetic diversity of the Papaya ringspot virus in Florida,” Proceedings of Florida State Horticulture Society, vol. 112, pp. 194–196, 1999. View at Google Scholar
  65. M. M. M. Fitch, “Carica papaya Papaya,” in Biotechnology of Fruit and Nut Crops, R. E. Litz, Ed., Capter 6.1, pp. 174–207, CABI publishing, 2005. View at Google Scholar
  66. C. Gonsalves, W. Cai, P. F. Tennant, and D. Gonsalves, “Effective development of papaya ringspot virus resistant papaya with untranslatable coat protein gene using a modified microprojectile transformation method,” Acta Horticulturae, vol. 461, pp. 311–319, 1998. View at Google Scholar
  67. H. J. Bau, Y. H. Cheng, T. A. Yu et al., “Field evaluation of transgenic papaya lines carrying the coat protein gene of Papaya ringspot virus in Taiwan,” Plant Disease, vol. 88, no. 6, pp. 594–599, 2004. View at Publisher · View at Google Scholar
  68. P. M. Magdalita, L. D. Valencia, A. T. I. D. Ocampo et al., “Towards development of PRSV resistant papaya by genetic engineering. In: New Directions for a Diverse Planet,” in Proceedings of the 4th International Crop Science Congress, Brisbane, Australia, October, 2004.
  69. P. M. Waterhouse, M. W. Graham, and M.-B. Wang, “Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 23, pp. 13959–13964, 1998. View at Publisher · View at Google Scholar · View at Scopus
  70. A. Eamens, M.-B. Wang, N. A. Smith, and P. M. Waterhouse, “RNA silencing in plants: yesterday, today, and tomorrow,” Plant Physiology, vol. 147, no. 2, pp. 456–468, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. S. V. Ramesh, A. K. Mishra, and S. Praveen, “Hairpin RNA-mediated strategies for silencing of tomato leaf curl virus AC1 and AC4 genes for effective resistance in plants,” Oligonucleotides, vol. 17, no. 2, pp. 251–257, 2007. View at Publisher · View at Google Scholar · View at Scopus
  72. S.-D. Yeh, F.-J. Jan, C.-H. Chiang et al., “Complete nucleotide sequence and genetic organization of papaya ringspot virus RNA,” Journal of General Virology, vol. 73, no. 10, pp. 2531–2541, 1992. View at Google Scholar · View at Scopus
  73. P. Ruanjan, S. Kertbundit, and M. Juříček, “Post-transcriptional gene silencing is involved in resistance of transgenic papayas to papaya ringspot virus,” Biologia Plantarum, vol. 51, no. 3, pp. 517–520, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. S. K. Mangrauthia, R. K. Jain, and S. Praveen, “Sequence motifs comparisons establish a functional portrait of a multifunctional protein HC-Pro from papaya ringspot potyvirus,” Journal of Plant Biochemistry and Biotechnology, vol. 17, no. 2, pp. 201–204, 2008. View at Google Scholar · View at Scopus
  75. J. Meins F., “RNA degradation and models for post-transcriptional gene silencing,” Plant Molecular Biology, vol. 43, no. 2-3, pp. 261–273, 2000. View at Google Scholar · View at Scopus
  76. M. Wassenegger and T. Pélissier, “A model for RNA-mediated gene silencing in higher plants,” Plant Molecular Biology, vol. 37, no. 2, pp. 349–362, 1998. View at Publisher · View at Google Scholar · View at Scopus
  77. P. Tennant, G. Fermin, M. M. Fitch, R. M. Manshardt, J. L. Slightom, and D. Gonsalves, “Papaya ringspot virus resistance of transgenic rainbow and SunUp is affected by gene dosage, plant development, and coat protein homology,” European Journal of Plant Pathology, vol. 107, no. 6, pp. 645–653, 2001. View at Publisher · View at Google Scholar · View at Scopus
  78. S. Tripathi, H.-J. Bau, L.-F. Chen, and S.-D. Yeh, “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,” European Journal of Plant Pathology, vol. 110, no. 9, pp. 871–882, 2004. View at Publisher · View at Google Scholar · View at Scopus
  79. D. B. Golemboski, G. P. Lomonossoff, and M. Zaitlin, “Plants transformed with a tobacco mosaic virus nonstructural gene sequence are resistant to the virus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 16, pp. 6311–6315, 1990. View at Publisher · View at Google Scholar · View at Scopus
  80. T. Nunome, F. Fukumoto, F. Terami, K. Hanada, and M. Hirai, “Development of breeding materials of transgenic tomato plants with a truncated replicase gene of cucumber mosaic virus for resistance to the virus,” Breeding Science, vol. 52, no. 3, pp. 219–223, 2002. View at Publisher · View at Google Scholar · View at Scopus
  81. X. Wei, C. Lan, Z. Lu, and C. Ye, “Analysis on virus resistance and fruit quality for T4 generation of transgenic papaya,” Frontiers of Biology in China, vol. 2, no. 3, pp. 284–290, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Sakuanrungsirikul, N. Sarindu, V. Prasartsee et al., “Update on the development of virus-resistant papaya: virus-resistant transgenic papaya for people in rural communities of Thailand,” Food and Nutrition Bulletin, vol. 26, no. 4, pp. 422–426, 2005. View at Google Scholar · View at Scopus
  83. Y.-T. Hsieh and T.-M. Pan, “Influence of planting papaya ringspot virus resistant transgenic papaya on soil microbial biodiversity,” Journal of Agricultural and Food Chemistry, vol. 54, no. 1, pp. 130–137, 2006. View at Publisher · View at Google Scholar · View at Scopus
  84. M. Roberts, D. A. Minott, P. F. Tennant, and J. C. Jackson, “Assessment of compositional changes during ripening of transgenic papaya modified for protection against papaya ringspot virus,” Journal of the Science of Food and Agriculture, vol. 88, no. 11, pp. 1911–1920, 2008. View at Publisher · View at Google Scholar · View at Scopus
  85. R. Stone, “China plans $3.5 billion GM crops initiative,” Science, vol. 321, no. 5894, p. 1279, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. C. Gonsalves, D. R. Lee, and D. Gonsalves, “The adoption of genetically modified papaya in Hawaii and its implications for developing countries,” Journal of Development Studies, vol. 43, no. 1, pp. 177–191, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. G. Fermin, V. Inglessis, C. Garboza, S. Rangel, M. Dagert, and D. Gonsalves, “Engineered resistance against Papaya ringspot virus in Venezuelan transgenic papayas,” Plant Disease, vol. 88, no. 5, pp. 516–522, 2004. View at Google Scholar · View at Scopus
  88. N. Phironrit, B. Phuangrat, P. Burns, and W. Kositratana, “Determination of possible impact on the cultivation of PRSV resistant transgenic papaya to rhizosphere bacteria using the community-level physiological profiles (CLPP),” in Proceedings of the 6th Asian Crop Science Association Conference, p. 126, Bangkok, Thailand, November 2007.
  89. R. Manshardt, “Is organic papaya production in Hawaii threatened by crosspollination with genetically engineered varieties,” University of Hawaii College Tropical Agriculture and Human Resource Biology, vol. 3, p. 2, 2002. View at Google Scholar
  90. S. D. Yeh and D. Gonsalves, “Practices and perspective of control of papaya ringspot virus by cross protection,” in Advances in Disease Vector Research, K. F. Harris, Ed., vol. 10, pp. 237–257, Springer, New York, NY, USA, 1994. View at Google Scholar
  91. G. Fermín, R. C. Keith, J. Y. Suzuki et al., “Allergenicity assessment of the papaya ringspot virus coat protein expressed in transgenic rainbow papaya,” Journal of Agricultural and Food Chemistry, vol. 59, no. 18, pp. 10006–10013, 2011. View at Publisher · View at Google Scholar · View at Scopus
  92. H. T. Lin, G. C. Yen, T. T. Huang, L. F. Chan, and et. al, “Toxicity assessment of transgenic papaya ringspot virus of 823–2210 line papaya fruits,” Journal of Agricultural and Food Chemistry, vol. 61, no. 7, pp. 1585–1596, 2013. View at Google Scholar
  93. M. G. Ettlinger and A. Kjaer, “Sulfur compounds in plants,” Recent Advances in Phytochemistry, vol. 1, pp. 49–144, 1968. View at Google Scholar
  94. S. S. Hecht, P. M. J. Kenney, M. Wang, and P. Upadhyaya, “Benzyl isothiocyanate: an effective inhibitor of polycyclic aromatic hydrocarbon tumorigenesis in A/J mouse lung,” Cancer Letters, vol. 187, no. 1-2, pp. 87–94, 2002. View at Publisher · View at Google Scholar · View at Scopus
  95. G. Fermin and P. Tennant, “Opportunities and constraints to biotechnological applications in the Caribbean: transgenic papayas in Jamaica and Venezuela,” Plant Cell Reports, vol. 30, no. 5, pp. 681–687, 2011. View at Publisher · View at Google Scholar · View at Scopus
  96. A. C. Lima, R. Souza Jr., T. Monoel, R. Gilvan, and A. A. Lima, “Sequence of the coat protein gene from Brazilian isolates of papaya ringspot virus,” Fitopatologia Brasileira, vol. 27, pp. 263–267, 2002. View at Google Scholar
  97. M. T. Souza, O. Nickel, and D. Gonsalves, “Development of virus resistant transgenic papayas expressing the coat protein gene from a Brazilian isolate of papaya ringspot virus,” Fitopatologia Brasileira, vol. 30, pp. 357–365, 2005. View at Google Scholar
  98. M. J. Davis and Z. Ying, “Development of papaya breeding lines with transgenic resistance to Papaya ringspot virus,” Plant Disease, vol. 88, no. 4, pp. 352–358, 2004. View at Google Scholar · View at Scopus
  99. P. Tennant, M. H. Ahmad, and D. Gonsalves, “Field resistance of coat protein transgenic papaya to Papaya ringspot virus in Jamaica,” Plant Disease, vol. 89, no. 8, pp. 841–847, 2005. View at Publisher · View at Google Scholar · View at Scopus
  100. S. A. Ferreira, K. Y. Pitz, R. Manshardt, M. Fitch, and D. Gonsalves, “Virus coat protein transgenic papaya provides practical control of Papaya ringspot virus in Hawaii,” Plant Disease, vol. 86, no. 2, pp. 101–105, 2002. View at Google Scholar · View at Scopus
  101. G. Fermin, Use, application and technology transfer of native and synthetic genes to engineering single and multiple transgenic viral resistance [Ph.D. thesis], Cornell University, Ithaca, NY, USA, 2002.
  102. S. Kertbundit, N. Pongtanom, P. Ruanjan et al., “Resistance of transgenic papaya plants to Papaya ringspot virus,” Biologia Plantarum, vol. 51, no. 2, pp. 333–339, 2007. View at Publisher · View at Google Scholar · View at Scopus