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Transgene-mediated resistance to Papaya ringspot virus: challenges and solutions

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Abstract

Global papaya production is severely affected by papaya ringspot disease caused by Papaya ringspot virus (PRSV). Management of this potyvirus is challenging, due to 1) its non-persistent transmission by numerous aphid species and 2) the diversity of PRSV strains that exists within a country or between different geographical regions. Papaya cultivars with transgenic resistance have reduced the impact of the disease. There are no effective alternatives to transgenic resistance available in areas where disease pressure is high. In Hawaii, transgenic papayas such as “SunUp” and “Rainbow” have remained resistant to PRSV more than two decades saving the commercial papaya industry. Following the success in Hawaii, researchers from other countries have focused on developing PRSV-resistant transgenic papaya. These transgenic cultivars often demonstrated an initial transitory resistance that was ultimately overcome by the virus. For other cases, resistance was inconsistent. That is, some transgenic lines were resistant while others were not. Transgenic cultivars are now losing PRSV-resistance for various reasons in China and Taiwan. In this review, we present an update on work with transgenic papaya with resistance to PRSV. The focus is on factors affecting transgenic resistance in papaya and our attempt to explain why the Hawaiian scenario of complete and durable resistance has not been replicated in other regions. The utilization of more recent technologies to the development of virus resistance in papaya is also discussed.

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References

  • Adams, M. J., Antoniw, J. F., & Beaudoin, F. (2005). Review: overview and analysis of the polyprotein cleavage sites in the family Potyviridae. Molecular Plant Pathology, 6, 471–487. https://doi.org/10.1111/j.1364-3703.2005.00296.x.

    Article  CAS  PubMed  Google Scholar 

  • Agrawal, N., Dasaradhi, P. V. N., Mohmmed, A., Malhotra, P., Bhatnagar, R. K., & Mukherjee, S. K. (2003). RNA interference: biology, mechanism, and applications. Microbiology and Molecular Biology Reviews, 67(4), 657–685. https://doi.org/10.1128/MMBR.67.4.657-685.2003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alabi, O. J., Al Rwahnih, M., Brown, J. K., Idris, A. M., Gregg, L., Kmieciak, E., Sétamou, M., & Jifon, J. L. (2016). First report of papaya (Carica papaya) naturally infected with the introduced Tomato yellow leaf curl virus-Israel. Plant Disease, 100(9), 1959. https://doi.org/10.1094/PDIS-04-16-0469-PDN.

    Article  Google Scholar 

  • Ali, Z., Abul-faraj, A., Idris, A., Ali, S., Tashkandi, M., & Mahfouz, M. M. (2015). CRISPR/Cas9-mediated viral interference in plants. Genome Biology, 16, 1–11. https://doi.org/10.1186/s13059-015-0799-6.

    Article  CAS  Google Scholar 

  • Anandalakshmi, R., Pruss, G. J., Ge, X., Marathe, R., Mallor, A. C., Smith, T. H., & Vance, V. B. (1998). A viral suppressor of gene silencing in plants. Proceedings of the National Academy of Sciences, 95(22), 13079–13084. https://doi.org/10.1073/pnas.95.22.13079.

    Article  CAS  Google Scholar 

  • Azad, M. A. K., Amin, L., & Sidik, N. M. (2014). Gene technology for Papaya ringspot virus disease management. The Scientific World Journal. https://doi.org/10.1155/2014/768038.

  • Badillo, V. (1993). Caricaceae, segundo esquema. Revista de la Facultad de Agronornia (Maracay), 43, 111.

    Google Scholar 

  • Baltes, N. J., Hummel, A. W., Konecna, E., Cegan, R., Bruns, A. N., Bisaro, D. M., & Voytas, D. F. (2015). Conferring resistance to geminiviruses with the CRISPR-Cas prokaryotic immune system. Nature Plants, 1, 15145. https://doi.org/10.1038/nplants.2015.145.

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.1094/PHYTO.2003.93.1.112.

    Article  CAS  PubMed  Google Scholar 

  • Bau, H. J., Cheng, Y. H., Yu, T. A., Yang, J. S., Liou, P. C., Hsiao, C. H., Lin, C. Y., & Yeh, S. D. (2004). Field evaluation of transgenic papaya lines carrying the coat protein gene of Papaya ringspot virus in Taiwan. Plant Disease, 85, 594–599.

    Article  Google Scholar 

  • Bau, H. J., Kung, Y. J., Raja, J., Chan, S. J., Chen, K. C., Chen, Y. K., Wu, H. W., & Yeh, S. D. (2008). Potential threat of a new pathotype of Papaya leaf distortion mosaic virus infecting transgenic papaya resistant to Papaya ringspot virus. Phytopathology, 98, 848–856. https://doi.org/10.1094/PHYTO-98-7-0848.

    Article  CAS  PubMed  Google Scholar 

  • Baulcombe, D. C. (1996). RNA as a target and an initiator of post-transcriptional gene silencing in transgenic plants. Plant Molecular Biology, 32, 79–88.

    Article  CAS  PubMed  Google Scholar 

  • Baulcombe, D., English, J., Mueller, E., & Davenport, G. (1996). Gene silencing and virus resistance in transgenic plants. In G. W. Grierson, G. W. Lycett, & G. A. Tucker (Eds.), Mechanisms and applications of gene silencing (pp. 127–138). Nottingham: Nottingham University Press.

    Google Scholar 

  • Beachy, R. N. (1997). Mechanisms and applications of pathogen-derived resistance in transgenic plants. Current Opinion Biotechnoogy, 8, 215–220.

    Article  CAS  Google Scholar 

  • Bonfim, K., Faria, J. C., Nogueira, E. O., Mendes, E. A., & Aragão, F. J. L. (2007). RNAi-mediated resistance to Bean golden mosaic virus in genetically engineered common bean (Phaseolus vulgaris). Molecular Plant Microbe Interaction., 20(6), 717–726.

    Article  CAS  Google Scholar 

  • Calvert, L. A., & Ghabrial, S. A. (1983). Enhancement by soybean mosaic virus of bean pod mottle virus titer in doubly infected soybean. Phytopathology, 73, 992–997.

    Article  Google Scholar 

  • Carvalho, F. D., Gheysen, G., Kushnir, S. M., Inze, D., & Castresana, C. (1992). Suppression of beta-1,3-glucanase transgene expression in homozygous plants. European Molecular Biology Organization Journal, 11, 2595–2602.

    Google Scholar 

  • Chan Jr., H. T., & Tang, C.-S. (1979). The chemistry and biochemistry of papaya. In G. E. Inglett & G. Charolambous (Eds.), Tropical foods: Chemistry and nutrition (Vol. 1, pp. 33–53). New York: Academic press.

    Chapter  Google Scholar 

  • Chandrasekaran, J., Brumin, M., Wolf, D., Leibman, D., Klap, C., Pearlsman, M., Sherman, A., Arazi, T., & Gal-On, A. (2016). Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Molecular Plant Pathology, 17(7), 1140–1153. https://doi.org/10.1111/mpp.12375.

    Article  CAS  PubMed  Google Scholar 

  • Chaves-Bedoya, G., & Ortiz-Rojas, L. Y. (2015). Genetic variability of papaya ringspot virus isolates in Norte de Santander - Colombia. Agronomia Colombiana, 33(2), 184–193.

    Article  Google Scholar 

  • Chen, G., Ye, C., Huang, J., Yu, M., & Li, B. (2001). 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, 20(3), 272–277.

    Article  CAS  Google Scholar 

  • 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 Report, 16, 127–132. https://doi.org/10.1007/BF01890852.

    Article  CAS  Google Scholar 

  • 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. Journal of General Virology, 82, 2827–2836. https://doi.org/10.1099/0022-1317-82-11-2827.

    Article  CAS  PubMed  Google Scholar 

  • Chung, B. Y. W., Miller, W. A., Atkins, J. F., & Firth, A. E. (2008). An overlapping essential gene in the Potyviridae. Proceedings of the National Academy of Sciences of the United States of America, 105, 5897–5902.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cruz, F. C. S., Tanada, J. M., Elvira, P. R. V., Dolores, L. M., Magdalita, P. M., Hautea, D. M., & Hautea, R. A. (2009). Detection of mixed virus infection with Papaya ringspot virus (PRSV) in papaya (Carica papaya L.) grown in Luzon, Philippines. Philippine Journal of Crop Science, 34, 62–74.

    Google Scholar 

  • Daltro, C. B., Pereira, Á. J., Cascardo, R. S., Alfenas-Zerbini, P., Bezerra-Junior, J. E. A., Lima, J. A. A., Zerbini, F. M., & Andrade, E. C. (2012). Genetic variability of papaya lethal yellowing virus isolates from Ceará and Rio Grande do Norte states, Brazil. Tropical Plant Pathology, 37(1), 37–43.

    Article  Google Scholar 

  • Davis, M. J., & Ying, Z. (2004). Development of papaya breeding lines with transgenic resistance to Papaya ringspot virus. Plant Disease, 88, 352–358. https://doi.org/10.1094/PDIS.2004.88.4.352.

    Article  CAS  Google Scholar 

  • Dey, K. K., Hong, L., Borth, W. B., Melzer, M. J., & Hu, J. S. (2012). A highly sensitive single-tube nested PCR assay for the detection of Pineapple mealybug wilt associated virus-2 (PMWaV-2). Journal of Virological Methods, 183, 215–218.

    Article  CAS  PubMed  Google Scholar 

  • Dıaz-Pendon, J. A., & Ding, S. W. (2008). Direct and indirect roles of viral suppressors of RNA silencing in pathogenesis. Annual Review of Phytopathology, 46, 303–326. https://doi.org/10.1146/annurev.phyto.46.081407.104746.

    Article  PubMed  CAS  Google Scholar 

  • Ding, S. W., & Voinnet, O. (2007). Antiviral immunity directed by small RNAs. Cell, 130, 413–426. https://doi.org/10.1016/j.cell.2007.07.039.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duprat, A., Caranta, C., Revers, F., Menand, B., Browning, K. S., & Robaglia, C. (2002). The Arabidopsis eukaryotic initiation factor (iso)4E is dispensable for plant growth but required for susceptibility to potyviruses. Plant Journal., 32, 927–934.

    Article  CAS  PubMed  Google Scholar 

  • Fagard, M., & Vaucheret, H. (2000). (Trans) gene silencing in plants: how many mechanisms? Annual Review of Plant Physiology and Plant Molecular Biology, 51, 167–194.

    Article  CAS  PubMed  Google Scholar 

  • FAOSTAT. (2014). Production. http://faostat.fao.org/site/339/default.aspx. Accessed 19 Dec 2014.

  • Fermin, G., & Gonsalves, D. (2001). Towards the development of short synthetic genes for multiple virus resistance. Phytopathology, 91, 28.

    Google Scholar 

  • Fermin, G., & Gonsalves, D. (2004). Control of viral diseases of papaya: Native, chimeric and synthetic transgenes to engineer resistance against Papaya ringspot virus. In G. Loebenstein & G. Thottappilly (Eds.), Virus and virus-like diseases of major crops in developing coutries (pp. 497–518). The Netherlands: Kluwer Academic Press Publishers.

    Google Scholar 

  • Fermin, G. A., & Randle, M. (2015). Papaya ringspot. In P. Tennant & G. A. Fermin (Eds.), Virus diseases of tropical and subtropical crops. London: Cabi.

    Google Scholar 

  • Fermin, G. A., Inglesses, V., Garbozo, C., Rangel, S., Dagert, M., & Gonsalves, D. (2004). Engineered resistance against PRSV in Venezuelan transgenic papayas. Plant Disease, 88, 516–522.

    Article  Google Scholar 

  • Fermin, G. A., Castro, L. T., & Tennant, P. F. (2010). CP-transgenic and non-transgenic approaches for the control of papaya ringspot: current situation and challenges. Transgenic Plant Journal, 4, 1–15.

    Google Scholar 

  • Fermin-Munoz, G. A. (2002). Use, application, and technology transfer of native and synthetic genes for engineering single and multiple transgenic viral resistances (p. 293). Ithaca: Department of Plant Pathology, Cornell University.

    Google Scholar 

  • Ferreira, S., Mau, R., Manshardt, R., Pitz, K., & Gonsalves, D. (1992). Field evaluation of papaya ringspot virus cross protection. In Proc. 28th Annual Hawaii Papaya Industry Association Conference (pp. 29–30).

  • Ferreira, S. A., Pitz, K. Y., Manshardt, R., Fitch, M., & Gonsalves, D. (2002). Virus coat protein transgenic papaya provides practical control of Papaya ringspot virus in Hawaii. Plant Disease, 86(2), 101–105.

    Article  Google Scholar 

  • Fitch, M. M. M. (2010). Papaya ringspot virus (PRSV) resistance in papaya: update on progress worldwide. Transgenic Plant Journal, 4, 16–28.

    Google Scholar 

  • Fitch, M. M., & Manshardt, R. M. (1990). Somatic embryogenesis and plant regeneration from immature zygotic embryos of papaya (Carica papaya L.) Plant Cell Reports, 9, 320–324. https://doi.org/10.1007/BF00232860.

    CAS  PubMed  Google Scholar 

  • Fitch, 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. https://doi.org/10.1038/nbt1192-1466.

    CAS  Google Scholar 

  • Fuchs, M., & Gonsalves, D. (2007). Safety of virus-resistant transgenic plants two decades after their introduction: lessons from realistic field risk assessment studies. Annual Review of Phytopathology, 45, 173–202. https://doi.org/10.1146/annurev.phyto.45.062806.094434.

    Article  CAS  PubMed  Google Scholar 

  • Gómez, P., Rodríguez-Hernández, A. M., Moury, B., & Aranda, M. A. (2009). Genetic resistance for the sustainable control of plant virus diseases: breeding, mechanisms and durability. European Journal of Plant Pathology, 125, 1–22.

    Article  Google Scholar 

  • Gonsalves, D. (1998). Control of papaya ringspot virus in papaya: a case study. Annual Review of Phytopathology, 36, 415–437. https://doi.org/10.1146/annurev.phyto.36.1.415.

    Article  CAS  PubMed  Google Scholar 

  • Gonsalves, D. (2002). Coat protein transgenic papaya: “acquired” immunity for controlling Papaya ringspot virus. Current Topics in Microbiology and Immunology, 266, 73–83. https://doi.org/10.1007/BF00232860.

    CAS  PubMed  Google Scholar 

  • Gonsalves, D. (2004). Tansgenic papaya in Hawaii and beyond. AgBioforum, 7(1&2), 36–40.

    Google Scholar 

  • Gonsalves, D., Gonsalves, C., Ferreira, S., Pitz, K., Fitch, M., Manshardt, R., & Slightom, J. (2004). Transgenic virus resistant papaya: From hope to reality for controlling papaya ringspot virus in Hawaii. APSnetFeatures, http://www.apsnet.org/online/feature/ringspot/. https://doi.org/10.1094/APSnetFeature-2004-0704.

  • Green, J. C., & Hu, S. J. (2017). Editing plants for virus resistance using CRISPR-Cas. Acta Virologica, 61, 138–142. https://doi.org/10.4149/av_2017_02_02.

    Article  CAS  PubMed  Google Scholar 

  • Guo, J., Yang, L., Liu, X., Guan, X., Jiang, L., & Zhang, D. (2009). Characterization of the exogenous insert and development of event-specific PCR detection methods for genetically modified Huanong No. 1 papaya. Journal of Agricultural and Food Chemistry, 57, 7205–7212. https://doi.org/10.1021/jf901198x.

    Article  CAS  PubMed  Google Scholar 

  • Hamim, I., Alam, M. Z., Ali, M. A., & Ashrafuzzaman, M. (2014). Incidence of post-harvest fungal diseases of ripe papaya in Mymensingh. Journal of Bangladesh Agricultural University, 12(1), 25–28.

    Article  Google Scholar 

  • Hamim, I., Borth, W., Melzer, M. J., Green, J. C., & Hu, J. (2017). Detection of Papaya ringspot virus using an ultra-sensitive single-tube nested PCR. 29 th annual CTAHR and COE student research symposium. University of Hawai‘i at Mānoa, USA

  • Hanley-Bowdoin, L., Bejarano, E. R., Robertson, D., & Mansoor, S. (2013). Geminiviruses: masters at redirecting and reprogramming plant processes. Nature Reviews Microbiology, 11, 777–788. https://doi.org/10.1038/ nrmicro3117.

    Article  CAS  PubMed  Google Scholar 

  • Hsu, P. D., Lander, E. S., & Zhang, F. (2014). Development and applications of CRISPRCas9 for genome engineering. Cell, 157, 1262–1278.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jensen, D. D. (1949). Papaya virus diseases with special reference to papaya ringspot. Phytopathology, 39, 191–211.

    Google Scholar 

  • Ji, X., Zhang, H., Zhang, Y., Wang, Y., & Gao, C. (2015). Establishing a CRISPR-Cas-like immune system conferring DNA virus resistance in plants. Nature Plants, 1, 15144. https://doi.org/10.1038/nplants.2015.144.

    Article  CAS  PubMed  Google Scholar 

  • Jia, R., Zhao, H., Huang, J., Kong, H., Zhang, Y., Guo, J., Huang, Q., Guo, Y., Wei, Q., Zuo, J., Zhu, Y. J., Peng, M., & Guo, A. (2017). Use of RNAi technology to develop a PRSV-resistant transgenic papaya. Scientific Reports, 7(12636). https://doi.org/10.1038/s41598-017-13049-0.

  • Jiang, J., & Laliberté, J. F. (2011). The genome-linked protein VPg of plant viruses-a protein with many partners. Current Opinion Virology., 1, 347–354.

    Article  CAS  Google Scholar 

  • Kalantidis, K., Psaradakis, S., Tabler, M., & Tsagris, M. (2002). The occurrence of CMV specific short RNAs in transgenic tobacco expressing virus-derived doubles tranded RNA is indicative of resistance to the virus. Molecular Plant Microbe Interactions, 15, 826–833. https://doi.org/10.1094/MPMI.2002.15.8.826.

    Article  CAS  PubMed  Google Scholar 

  • Karyeija, R. F., Kreuze, J. F., Gibson, R. W., & Valkonen, J. P. (2000). Synergistic interactions of a potyvirus and a phloem-limited crinivirus in sweet potato plants. Virology, 269(1), 26–36.

    Article  CAS  PubMed  Google Scholar 

  • Kasschau, K. D., & Carrington, J. C. (1998). A Counter defensive strategy of plant viruses: suppression of post transcriptional gene silencing. Cell, 95, 461–470. https://doi.org/10.1016/S0092-8674(00)81614-1.

    Article  CAS  PubMed  Google Scholar 

  • Kos, M., Loon, J. J. V., Dicke, M., & Vet, L. E. M. (2009). Transgenic plants as vital components of integrated pest management. Trends in Biotechnology, 27(11), 621–627.

    Article  CAS  PubMed  Google Scholar 

  • Kung, Y. J., Bau, H. J., Wu, Y. L., Huang, C. H., Chen, T. M., & Yeh, S. D. (2009). Phytopathology, 99, 1312–1320. https://doi.org/10.1094/PHYTO-99-11-1312.

    Article  CAS  PubMed  Google Scholar 

  • Kung, Y., You, B., Raja, J. A. J., Chen, K., Huang, C., Bau, H., Yang, C., Huang, C., Chang, C., & Yeh, S. (2015). Nucleotide sequence-homology-independent breakdown of transgenic resistance by more virulent virus strains and a potential solution. Science Reports, 5, 9804. https://doi.org/10.1038/srep09804.

    Article  CAS  Google Scholar 

  • Lakatos, L., Csorba, T., Pantaleo, V., Chapman, E. J., Carrington, J. C., & Liu, Y. P. (2006). Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO Journal, 25, 2768–2780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lellis, A. D., Kasschau, K. D., Whitham, S. A., & Carrington, J. C. (2002). Loss of susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during Potyvirus Infection. Current Biology, 12, 1046–1051.

    Article  CAS  PubMed  Google Scholar 

  • Léonard, S., Plante, D., Wittmann, S., Daigneault, N., Fortin, M. G., & Laliberté, J. F. (2000). Complex formation between Potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. Journal of Virology, 74, 7730–7737.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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. Molecular Breeding, 10, 119–129. https://doi.org/10.1023/A:1020381110181.

    Article  CAS  Google Scholar 

  • 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. Biotechnology, 9, 752–758.

    CAS  PubMed  Google Scholar 

  • Lius, S., Manshardt, R. M., Fitch, M. M., Slightom, J. L., Sanford, J. C., & Gonsalves, D. (1997). Pathogen-derived resistance provides papaya with effective protection against papaya ringspot virus. Molecular Breeding, 3, 161–168.

    Article  Google Scholar 

  • Lu, Y. W., Shen, W. T., Zhou, P., Tang, Q. J., Niu, Y. M., Peng, M., & Xiong, Z. (2008). Complete genomic sequence of a papaya ringspot virus isolate from Hainan Island, China. Archives of Virology, 153, 991–993. https://doi.org/10.1007/s00705-008-0056-3.

    Article  CAS  PubMed  Google Scholar 

  • Mallory, A. C., Reinhart, B. J., Bartel, D., Vance, V. B., & Bowman, L. H. (2002). A viral suppressor of RNA silencing differentially regulates the accumulation of short interfering RNAs and micro-RNAs in tobacco. Proceedings of the National Academic of Sciences of the United States of America, 99, 15228–15233. https://doi.org/10.1073/pnas.232434999.

    Article  CAS  Google Scholar 

  • Mangrauthia, S. K., Parameswari, B., Jain, R. K., & Praveen, S. (2008). Role of genetic recombination in the molecular architecture of papaya ringspot virus. Biochemical Genetics, 46(11–12), 835–846. https://doi.org/10.1007/s10528-008-9198-y.

    Article  CAS  PubMed  Google Scholar 

  • Mangrauthia, S. K., Shakya, V. P. S., Jain, R. K., & Praveen, S. (2009). Ambient temperature perception in papaya for papaya ringspot virus interaction. Virus Genes, 38, 429–434. https://doi.org/10.1007/s11262-009-0336-3.

    Article  CAS  PubMed  Google Scholar 

  • Mangrauthia, S. K., Priyanka, S. E., & Praveen, E. S. (2010). Genomics of helper component proteinase reveals effective strategy for Papaya Ringspot Virus resistance. Molecular Biotechnology, 44, 22–29. https://doi.org/10.1007/s12033-009-9205-5.

    Article  CAS  PubMed  Google Scholar 

  • Manshardt, R. M. (1999). ‘UH Rainbow’ papaya a high-quality hybrid with genetically engineered disease resistance. University of Hawaii College of Tropical Agriculture and Human Resources(CTAHR), New Plants for Hawaii (NPH)-1, revised. Available at: http://www.ctahr.hawaii.edu/ctahr200l/P]O/FreePubs/FreePubsO7.asp#NewPlantsForHawaii.

  • Mansoor, S., Khan, S. H., Bashir, A., Saeed, M., Zafar, Y., Malik, K. A., et al. (1999). Identification of a novel circular single-stranded DNA associated with cotton leaf curl disease in Pakistan. Virology, 259, 190–199. https://doi.org/10.1006/viro.1999.9766

    Article  CAS  PubMed  Google Scholar 

  • Matzke, M. A., & Matzke, A. J. M. (1998). Epigenetic silencing of plant transgenes as a consequence of diverse cellular defence responses. Cellular and Molecular Life Sciences, 54, 94–103.

    Article  CAS  PubMed  Google Scholar 

  • Mazier, M., Flamain, F., Nicolaï, M., Sarnette, V., & Caranta, C. (2011). Knock-down of both eIF4E1 and eIF4E2 genes confers broad-spectrum resistance against Potyviruses in Tomato. PLoS One, 6, e29595.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendoza, T. E. M., Laurena, A., & Botella, J. R. (2008). Recent advances in the development of transgenic papaya technology. Biotechnology Annual Review, 14, 423–462. https://doi.org/10.1016/S1387-2656(08)00019-7.

    Article  CAS  Google Scholar 

  • Merai, Z., Kerenyi, Z., Kertesz, S., Magna, M., Lakatos, L., & Silhavy, D. (2006). Double-stranded RNA binding may be a general plant viral strategy to suppress RNA silencing. Journal of Virology, 80, 5747–5756.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moffat, A. S. (1999). Geminiviruses emerge as serious crop threat. Science, 286, 1835.

    Article  CAS  Google Scholar 

  • Murphy, J. F., & Bowen, K. L. (2006). Synergistic disease in pepper caused by the mixed infection of Cucumber mosaic virus and Pepper mottle virus. Phytopathology, 96, 240–247.

    Article  PubMed  Google Scholar 

  • Namba, R., & Higa, S. Y. (1981). Papaya mosaic transmission as affected by the duration of the acquisition probe of the green peach aphid – Myzus persicae (Sulzer). Proceeding of Hawaiian Entomology Society, 23, 431–443.

    Google Scholar 

  • Nicaise, V., German-Retana, S., Sanjuán, R., Dubrana, M. P., Mazier, M., Maisonneuve, B., Candresse, T., Caranta, C., & LeGall, O. (2003). The eukaryotic translation initiation factor 4E controls Lettuce susceptibility to the Potyvirus Lettuce mosaic virus. Plant Physiology, 132, 1272–1282.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noa-Carrazana, J., González-de-León, D., Ruiz-Castro, B., Piñero, D., & Silva-Rosales, L. (2006). Distribution of Papaya ringspot virus and Papaya mosaic virus in papaya plants (Carica papaya) in Mexico. Plant Disease, 90, 1004–1011. https://doi.org/10.1094/PD-90-1004.

    Article  Google Scholar 

  • Ohshima, K., Tomitaka, Y., Wood, J. T., Minematsu, Y., Kajiyama, H., Tomimura, K., & Gibbs, A. J. (2007). Pattern of recombination in Turnip mosaic virus genomic sequences indicates hotspots of recombination. Journal of General Virology., 88, 298–315.

    Article  CAS  PubMed  Google Scholar 

  • Paolla, M. V. A., Tathiana, F. S. A., Anuar, M. Á., Daisy, P. B., Raúl, T. T., José, A. V., Antonio, A. R. F., & Patricia, M. B. F. (2015). A current overview of the Papaya meleira virus, an unusual plant virus. Virus, 7, 1853–1870. https://doi.org/10.3390/v7041853.

    Article  CAS  Google Scholar 

  • Phironrit, N., Chowpongpang, S., Warin, N., Bhunchoth, A., & Attathom, S. (2005). Small scale field testing of PRSV resistance in transgenic papaya line KN116/5. In I International Symposium on Papaya 740 (pp. 169–176).

  • Powell-Abel, P., Nelson, R. S., De, B., Hoffmann, N., & Rogers, S. G. (1986). Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science, 232, 738–743. https://doi.org/10.1126/science.232.4751.738.

    Article  Google Scholar 

  • Prasad, S. M., & Sarkar, D. P. (1989). Some ecological studies on Papaya ringspot virus in Ranchi. Indian Journal Virology, 5, 118–122.

    Google Scholar 

  • Pruss, G., Ge, X., Shi, X. M., Carrington, J. C., & Vance, V. B. (1997). Plant viral synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. The Plant Cell, 9, 859–868. https://doi.org/10.1105/tpc.9.6.859.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Purcifull, D., Edwardson, J., Hiebert, F., & Gonsalves, D. (1984). Papaya ringspot virus. CM1/AAB Descriptions of Plant Viruses. No. 292. (No. 64 Revised, July 1984), pp. 8.

  • Pyott, D. E., Sheehan, E., & Molnar, A. (2016). Engineering of CRISPR/Cas9-mediated potyvirus resistance in transgene-free Arabidopsis plants. Molecular Plant Pathology, 17, 1276–1288. https://doi.org/10.1111/mpp.12417.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quemada, H. L., Hostis, B., & Gonsalves, D. (1990). The nucleotide sequences of the 3′-terminal regions of papaya ringspot virus strains w and p. Journal of General Virology, 71, 203–210.

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Hernández, A. M., Gosalvez, B., Sempere, R. N., Burgos, L., Aranda, M. A., & Truniger, V. (2012). Melon RNA interference (RNAi) lines silenced for Cm-eIF4E show broad virus resistance. Molecular Plant Pathology., 13, 755–763.

    Article  PubMed  Google Scholar 

  • Ruanjan, P., Kertbundit, S., & Juricek, M. (2007). Post-transcriptional gene silencing is involved in resistance of transgenic papayas to papaya ringspot virus. Biologia Plantarum, 51, 517–520.

    Article  CAS  Google Scholar 

  • Ruffel, S., Gallois, J. L., Moury, B., Robaglia, C., Palloix, A., & Caranta, C. (2006). Simultaneous mutations in translation initiation factors eIF4E and eIF(iso)4E are required to prevent pepper veinal mottle virus infection of pepper. Journal of General Virology, 87, 2089–2098.

    Article  CAS  PubMed  Google Scholar 

  • Sakuanrungsirikul, S., Sarindu, N., Prasartsee, V., Chaikiatiyos, S., Siriyan, R., Sriwatanakul, M., Lekananon, P., Kitprasert, C., Boonsong, P., Kosiyachinda, P., Fermin, G., & Gonsalves, D. (2005). Update on the development of virus-resistant papaya: virus-resistant transgenic papaya forpeople in rural communities of Thailand. Food Nutrition Bulletin, 26, 422–426.

    Article  CAS  PubMed  Google Scholar 

  • Sanfaçon, H. (2015). Plant translation factors and virus resistance. Virus, 7, 3392–3419.

    Article  CAS  Google Scholar 

  • Sanford, J. C., & Johnston, S. A. (1985). The concept of parasite-derived resistance - Deriving resistance genes from the parasite’s own genome. Journal of Theoretical Biology, 113, 395–405.

    Article  Google Scholar 

  • Sato, M., Nakahara, K., Yoshii, M., Ishikawa, M., & Uyeda, I. (2005). Selective involvement of members of the eukaryotic initiation factor 4E family in the infection of Arabidopsis thaliana by potyviruses. FEBS Letter, 579, 1167–1171.

    Article  CAS  Google Scholar 

  • Schumann, U., Smith, N. A., Kazan, K., Michael, A. M., & Wang, M. B. (2013). Analysis of hairpin RNA transgene-induced gene silencing in Fusarium oxysporum. Silence, 4, 3. http://www.silencejournal.com/content/4/1/3. https://doi.org/10.1186/1758-907X-4-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Souza, M. T., Nickel, O., & Gonsalves, D. (2005a). Development of virus resistant transgenic papayas expressing the coat protein gene from a Brazilian isolate of papaya ringspot virus. Fitopatologia Brasileira, 30, 357–365.

    Article  Google Scholar 

  • Souza, J. M. T., Tennant, P. F., & Gonsalves, D. (2005b). Influence of coat protein transgene copy number on resistance in transgenic line 63–1 against papaya ringspot virus isolates. Hort- Science, 40, 2083–2087.

    Google Scholar 

  • Stokstad, E. (2008). Papaya takes on ringspot virus and wins. Science, 320, 472. https://doi.org/10.1126/science.320.5875.472.

    Article  CAS  PubMed  Google Scholar 

  • Sturrock, D. (1940). Tropical fruits for Southern Florida and Cuba and their uses. Jamaica Plain: The Arnold Arboretum of Harvard University.

    Google Scholar 

  • Swain, S., & Powell, D. (2001). Papaya ringspot virus resistant papaya: a case study. Online. University of Guelph. Available at http://www.foodsafetynetwork.ca/gmo/papayarep.Htm.

  • Tennant, P. F., Gonsalves, C., Ling, K. S., Fitch, M. M., Manshardt, R., Slightom, L. J., & Gonsalves, D. (1994). Differential protection against papaya ringspot virus isolates in coat protein gene transgenic papaya and classically cross-protected papaya. Phytopathology, 84(11), 1359–1366.

    Article  Google Scholar 

  • 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. European Journal of Plant Pathology, 107(6), 645–653. https://doi.org/10.1023/A:1017936226557.

    Article  CAS  Google Scholar 

  • Tennant, P. F., Ahmad, M. H., & Gonsalves, D. (2002). Transformation of Carica papaya L. with virus coat protein genes for studies on resistance to papaya ringspot virus from Jamaica. Tropical Agriculture (Trinidad), 79(2), 105–113.

    Google Scholar 

  • Tennant, P., Ahmad, M. H., & Gonsalves, D. (2005). Field resistance of coat protein transgenic papaya to Papaya ringspot virus in Jamaica. Plant Disease, 89, 841–847 apsjournals.apsnet.org/doi/pdf/10.1094/PD-89-0841.

    Article  CAS  Google Scholar 

  • Titanji, V. P. K., Zofou, D., & Ngemeneya, M. N. (2008). The Antimalarial potential of medicinal plants used for the treatment of malaria in Cameroonian Folk Medicine. The African Journal of Traditional, Complementary and Alternative Medicines, 5(3), 302–321.

    CAS  Google Scholar 

  • 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. European Journal of Plant Pathology, 110, 871–882. https://doi.org/10.1007/s10658-004-0607-8.

    Article  CAS  Google Scholar 

  • Tripathi, S., Suzuki, J. Y., Ferreira, S. A., & Gonsalves, D. (2008). Papaya ringspot virus - P: characteristics, pathogenicity, sequence variability and control. Molecular Plant Pathology, 9, 269–280. https://doi.org/10.1111/j.1364-3703.2008.00467.x.

    Article  CAS  PubMed  Google Scholar 

  • USDA/ARS. (2001). USDA nutrient data base for standard reference. Release 13.Nutrient Data Laboratory Home Page [online]. United States Department of Agriculture/Agricultural Research Service, 1999 [cited February 7, 2001]. Available from http:www.nal.usda.gov/fnic/foodcomp. accessed 17 Mar 2006.

  • Valli, A., Lopez-Moya, J. J., & Garcia, J. A. (2007). Recombination and gene duplication in the evolutionary diversification of P1 proteins in the family Potyviridae. The Journal of General Virology, 88, 1016–1028. https://doi.org/10.1099/vir.0.82402-0.

    Article  CAS  PubMed  Google Scholar 

  • Velázqueza, K., Renovella, A., Comellasa, M., Serraa, P., Garcı’ab, M. L., Pinaa, J. A., Navarroa, L., Morenoa, P., & Guerria, J. (2010). Effect of temperature on RNA silencing of a negative stranded RNA plant virus: Citrus psorosis virus. Plant Pathology, 59, 982–990.

    Article  CAS  Google Scholar 

  • Ventura, J. A., Costa, H., Tatagiba, J. S., Andrade, J. S., & Martins, D. S. (2003). Meleira do mamoeiro: Etiologia, sintomas e epidemiologia. In D. S. Martins (Ed.), Papaya Brasil: Qualidade do mamão para o mercado interno (pp. 267–276). Vitória: Incaper.

    Google Scholar 

  • Ventura, J. A., Costa, H., & da Silva Tatagiba, J. (2004). Papaya diseases and integrated control. In Diseases of fruits and vegetables (pp. 201–268). Berlin: Springer.

    Google Scholar 

  • Villegas, V. N., Magdalita, P. M., Valencia, L. D. & Ocampo, T. D. (2001). Development of transgenic papaya resistance to ringspot virus. Country progress report at the Papaya Biotechnology Network of Southeast Asia held in Hanoi, Vietnam, 22–23 October 2001.

  • Wang, H. L. (1981). Aphid transmission of Papaya ringspot virus in Taiwan. Plant Protection Bulletin, 23, 229–233.

    Google Scholar 

  • Wang, Y. N., Wu, B., Borth, W. B., Hamim, I., Green, J. C., Melzer, M. J., & Hu, J. S. (2017a). Molecular characterization and distribution of two strains of Dasheen mosaic virus on Taro in Hawaii. Plant Disease, 101(12), 1980–1989. https://doi.org/10.1094/PDIS-04-17-0516-RE.

    Article  Google Scholar 

  • Wang, Y. N., Borth, W. B., Green, J. C., Hamim, I., Cao, K., Hu, J. S., & Melzer, M. J. (2017b). Genome characterization and distribution of Taro bacilliform CH virus on taro in Hawaii, USA. European Journal of Plant Pathology, 387, 1–5.

    Google Scholar 

  • Ye, C., & Li, H. (2010). 20 years of transgenic research in China for resistance Papaya ringspot virus. Transgenic Plant Journal Global Science Book, 4(1), 58–63.

    Google Scholar 

  • Yeh, S. D., & Gonsalves, D. (1984). Evaluation of induced mutants of papaya ringspot virus for control by cross protection. Phytopathology, 74(9), 1086–1091.

    Article  Google Scholar 

  • Yeh, S. D., & Gonsalves, D. (1994). Practices and perspectives of control of papaya ringspot virus by cross protection. Advance Disease Vector Research, 10, 237–257.

    Article  Google Scholar 

  • Yeh, S. D., Jan, F. J., Chiang, C. H., Doong, T. J., Chen, M. C., Chung, P. H., & Bau, H. J. (1992). Complete nucleotide sequence and genetic organization of papaya ringspot virus RNA. Journal of General Virology, 73(10), 2531–2541. https://doi.org/10.1099/0022-1317-73-10-2531.

    Article  CAS  PubMed  Google Scholar 

  • Yeh, S., Bau, H., Cheng, Y., Yu, T., & Yang, J. (1998). Greenhouse and field evaluations of coat-protein transgenic papaya resistant to Papaya ringspot virus. Acta Horticulturae, (461, 461), 321–328. https://doi.org/10.17660/ActaHortic.1998.461.36

  • Yeh, S. D., Kung, Y. J., Bau, H. J., Yu, T. A., & Raja, J. A. J. (2010). Generation of a papaya hybrid variety with broad-spectrum transgenic resistance to papaya ringspot virus and papaya leaf-distortion mosaic virus. Transgenic Plant Journal., 4, 37–44.

    Google Scholar 

  • Yeh, S. D., Raja, J., Kung, Y.-J., & Kositratana, W. (2014). Agbiotechnology: costs and benefits of genetically modified papaya. In N. K. Van Alfen (Ed.), Encyclopedia of agriculture and food systems. London: Elsevier. https://doi.org/10.1016/B978-0-444-52512-3.00252-7.

    Google Scholar 

  • Zhang, Y., Yu, N., Huang, Q., Yin, G., Guo, A., Wang, X., Xiong, Z., & Liu, Z. (2014). Complete genome of Hainan papaya ringspot virus using small RNA deep sequencing. Virus Genes, 48, 502–508. https://doi.org/10.1007/s11262-014-1042-3.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, G., Yan, P., Shen, W., Tuo, D., Li, X., & Zhou, P. (2015). Complete genome sequence of papaya ringspot virus isolated from genetically modified papaya in Hainan island, China. Genome Announcements, 3(5), e01056–e01015. https://doi.org/10.1128/genomeA.01056-15.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao, H., Jia, R. Z., Zhang, Y. L., Zhu, Y. J., Zeng, H. C., Kong, H., McCafferty, H., Guo, A. P., & Peng, M. (2016). Geographical and genetic divergence among Papaya ringspot virus populations within Hainan Province, China. Phytopathology, 106(8), 937–944. https://doi.org/10.1094/PHYTO-05-15-0111-R Epub 2016 May 27.

    Article  CAS  PubMed  Google Scholar 

  • Zimmerman, T. W., Joseph, L., St. Brice, N., & Kowalski, J. A. (2005). Development and selection for homozygous transgenic papaya seedling. In I International Symposium on Papaya 740 (pp. 177–182).

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Acknowledgements

We appreciate the editorial suggestions of Dr. Stanley Freeman and Dr. Slavica Matic. This work was supported by the United States Agency for International Development, as part of the Feed the Future initiative, under the CGIAR Fund, award number BFS-G-1100002, and the predecessor fund of the Food Security and Crisis Mitigation II grant, award number EEM-G-0004-00013. The research is also supported by the USDA National Institute of Food and Agriculture, Hatch HAW09025-H (1001478), and the USDA-Agricultural Research Service (58-5320-4-012).

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Hamim, I., Borth, W.B., Marquez, J. et al. Transgene-mediated resistance to Papaya ringspot virus: challenges and solutions. Phytoparasitica 46, 1–18 (2018). https://doi.org/10.1007/s12600-017-0636-4

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