Expression of the Tomato pot-1 Gene Confers Potato Virus Y (PVY) Resistance in Susceptible Potato Varieties

American Journal of Potato Research volume 98, pages42–50(2021)Cite this article

Abstract

The translation initiation factor 4E (eIF4E) has been implicated in naturally-occurring resistance to the Potato Virus Y (PVY) determined by the pot-1 locus in tomato. The susceptible potato varieties Russet Norkotah, Silverton Russet, and Classic Russet, along with the Michigan State University breeding line MSE149-5Y, were transformed with the pot-1 gene from Solanum hirsutum to achieve PVY resistance. Transgenic potato events and their non-transgenic controls were screened for PVY resistance against three PVY strains (PVYO, PVYN:O, PVYNTN) by enzyme-linked immunosorbent assay (ELISA) in greenhouse and in field trials. The event A95.87.05 (Classic Russet) and MSE149.87.22 (MSE149-5Y) had resistance against all three PVY isolates tested in both foliage and tuber under either greenhouse or field conditions. In contrast, SR.87.62 (Silverton Russet) and RN1.87.09 (Russet Norkotah), displayed moderate susceptibility to PVY in foliage during the growing season and increased level of infection in tubers. Transformation of PVY-susceptible potato varieties with the tomato pot-1 gene can be a useful tool for improving PVY resistance.

Resumen

El factor de iniciación de traducción 4E (elF4E) se ha implicado en resistencia de ocurrencia natural al Virus Y de la Papa (PVY), determinado por el locus pot-1 en tomate. Las variedades susceptibles de papa Russet Norkotah, Silverton Russet y Classic Russet, junto con la línea de mejoramiento de la Universidad Estatal de Michigan MSE149-5Y, se transformaron con el gen pot-1 de Solanum hirsutum para lograr la resistencia al PVY. Los eventos de la papa transgénica y sus testigos no trangénicos se evaluaron para la resistencia a tres variantes del PVY (PVYO, PVY N:O, y PVY NTN) mediante serología de enzimas conjugadas (ELISA) en ensayos de invernadero y campo. Los eventos A95.87.05 (Classic Russet) y MSE149.87.22 (MSE149-5Y) tuvieron resistencia contra los tres aislamientos de PVY probados, tanto en follaje como en tubérculo, ya sea bajo condiciones de invernadero o de campo. En contraste, SR.87.62 (Silverton Russet) y RN1.87.09 (Russet Norkotah), mostraron susceptibilidad moderada al PVY en follaje durante el ciclo de cultivo y aumentaron el nivel de infección en tubérculos. La transformación de variedades de papa susceptibles al PVY con el gen pot-1 de tomate puede ser una herramienta útil para mejorar la resistencia al PVY.

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References

  1. Arcibal, E., K.M. Gold, S. Flaherty, J. Jiang, M. Jahn, and A.M. Rakotondrafara. 2016. A mutant eIF4E confers resistance to potato virus Y strains and is inherited in a dominant manner in the potato varieties Atlantic and russet Norkotah. American Journal of Potato Research 93: 64–71.

    CAS  Article  Google Scholar 

  2. Ayme, V., J. Petit-Pierre, S. Souche, A. Palloix, and B. Moury. 2007. Molecular dissection of the potato virus Y VPg virulence factor reveals complex adaptations to the pvr2 resistance allelic series in pepper. Journal of General Virology 88: 1594–1601.

    CAS  Article  Google Scholar 

  3. Cavatorta, J., K.W. Perez, S.M. Gray, J. Van Eck, I. Yeam, and M. Jahn. 2011. Engineering virus resistance using a modified potato gene. Plant Biotechnology Journal 9: 1014–1021.

    CAS  Article  Google Scholar 

  4. Collier, R., K. Dasgupta, Y. Xing, B.T. Hernandez, M. Shao, D. Rohozinski, E. Kovak, J. Lin, M.L.P. de Oliveira, E. Stover, K.F. McCue, F.G. Harmon, A. Blechl, J.G. Thomson, and R. Thilmony. 2017. Accurate measurement of transgene copy number in crop plants using droplet digital PCR. Plant Journal 90: 1014–1025.

    CAS  Article  Google Scholar 

  5. Diaz-Pendon, J.A., V. Truniger, C. Nieto, J. Garcia-Mas, A. Bendahmane, and M.A. Aranda. 2004. Advances in understanding recessive resistance to plant viruses. Molecular Plant Pathology 5: 223–233.

    CAS  Article  Google Scholar 

  6. Duan, H., C. Richael, and C.M. Rommens. 2012. Overexpression of the wild potato eIF4E-1 variant Eva1 elicits potato virus Y resistance in plants silenced for native eIF4E-1. Transgenic Research 21: 929–938.

    CAS  Article  Google Scholar 

  7. Gray, S., S. De Boer, J. Lorenzen, A. Karasev, J. Whitworth, P. Nolte, R. Singh, A. Boucher, and H. Xu. 2010. Potato virus Y: An evolving concern for potato crops in the United States and Canada. Plant Disease 94: 1384–1397.

    Article  Google Scholar 

  8. Gutierrez Sanchez, P.A., L. Babujee, H.J. Mesa, E. Arcibal, M. Gannon, D. Halterman, M. Jahn, J. Jiang, and A.M. Rakotondrafara. 2020. Overexpression of a modified eIF4E regulates potato virus y resistance at the transcriptional level in potato. BMC Genomics 21: 18.

    CAS  Article  Google Scholar 

  9. Hane, D.C., and P.B. Hamm. 1999. Effects of seedborne potato virus Y infection in two potato cultivars expressing mild disease symptoms. Plant Disease 83: 43–45.

    CAS  Article  Google Scholar 

  10. Hermsen, J.G. 1994. Introgression of genes from wild species, including molecular and cellular approaches. In Potato genetics, ed. J.E. Bradshaw, and G.R. Mackay, 515—538. Wallingford, UK: CAB International.

  11. Jackson, R.J., C.U.T. Hellen, and T.V. Pestova. 2010. The mechanism of eukaryotic translation initiation and principles of its regulation. Narure Reviews Molecullar Cell Biology 10: 113–127.

    Article  Google Scholar 

  12. Kang, B., I. Yeam, and M.M. Jahn. 2005. Genetics of plant virus resistance. Annual Review of Phytopathology 43: 581–621.

    CAS  Article  Google Scholar 

  13. Kang, B., I. Yeam, H. Li, K.W. Perez, and M.M. Jahn. 2007. Ectopic expression of a recessive resistance gene generates dominant potyvirus resistance in plants. Plant Biotechnology Journal 5: 526–536.

    CAS  Article  Google Scholar 

  14. Karasev, A.V., and S.M. Gray. 2013. Continuous and emerging challenges of potato virus Y in potato. Annual Review of Phytopathology 51: 571–586.

    CAS  Article  Google Scholar 

  15. Lebaron, C., A. Rosado, C. Sauvage, C. Gauffier, S. German-Retana, B. Moury, and J.L. Gallois. 2016. A new eIF4E1 allele characterized by RNAseq data mining is associated with resistance to potato virus Y in tomato albeit with a low durability. Journal of General Virology 97: 3063–3072.

    CAS  Article  Google Scholar 

  16. Legnani, R., K.G. Selassie, R.N. Womdim, P. Gognalons, A. Moretti, H. Laterrot, and G. Marchoux. 1995. Evaluation and inheritance of the Lycopersicon hirsutum resistance against potato virus Y. Tetrahedron Letters 11: 296–300.

    Google Scholar 

  17. Lellis, A.D., K.D. Kasschau, S.A. Whitham, and J.C. Carrington. 2002. Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for elF(iso)4E during potyvirus infection. Current Biology 12: 1046–1051.

    CAS  Article  Google Scholar 

  18. Li, W., K. Zarka, D.S. Douches, J.J. Coombs, W.L. Pett, and E.J. Grafius. 1999. Co-expression of potato PVYocoat protein gene and cryV-Bt genes in potato (Solanum tuberosum L.). Journal of the American Society for Horticultural Science 124 (3): 218–223.

  19. Mazier, M., F. Flamain, M. Nicolaï, V. Sarnette, and C. Caranta. 2011. Knock-down of both eIF4E1 and eIF4E2 genes confers broad-spectrum resistance against potyviruses in tomato. PLoS One 6 (12): e29595.

    CAS  Article  Google Scholar 

  20. Miroshnichenko, D., V. Timerbaev, A. Okuneva, A. Klementyeva, T. Sidorova, A. Pushin, and S. Dolgov. 2020. Enhancement of resistance to PVY in intragenic marker-free potato plants by RNAi-mediated silencing of eIF4E translation initiation factors. Plant Cell, Tissue and Organ Culture 140: 691–705.

    CAS  Article  Google Scholar 

  21. Murashige, T., and F. Skoog. 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15 (3): 473–497.

  22. Nie, B., M. Singh, A. Murphy, A. Sullivan, C. Xie, and X. Nie. 2012. Response of potato cultivars to five isolates belonging to four strains of potato virus Y. Plant Disease 96: 1422–1429.

    CAS  Article  Google Scholar 

  23. Parrella, G., S. Ruffel, A. Moretti, C. Morel, A. Palloix, and C. Caranta. 2002. Recessive resistance genes against potyviruses are localized in colinear genomic regions of the tomato (Lycopersicon spp.) and pepper (Capsicum spp.) genomes. Theoretical and Applied Genetics 105: 855–861.

    CAS  Article  Google Scholar 

  24. Patrick, R.M., and K.S. Browning. 2012. The eIF4F and eIFiso4F complexes of plants: An evolutionary perspective. Comparative and Functional Genomics Volume 2012, Article ID 287814.

  25. Piron, F., M. Nicolaï, S. Minoïa, E. Piednoir, A. Moretti, A. Salgues, D. Zamir, C. Caranta, and A. Bendahmane. 2010. An induced mutation in tomato eiF4E leads to immunity to two potyviruses. PLoS One 5 (6): e11313.

    Article  Google Scholar 

  26. Quenouille, J., N. Vassilakos, and B. Moury. 2013. Potato virus Y: A major crop pathogen that has provided major insights into the evolution of viral pathogenicity. Molecular Plant Pathology 14: 439–452.

    CAS  Article  Google Scholar 

  27. Robaglia, C., and C. Caranta. 2006. Translation initiation factors: A weak link in plant RNA virus infection. Trends in Plant Science 11: 40–45.

    CAS  Article  Google Scholar 

  28. Ruffel, S., M. Dussault, A. Palloix, B. Moury, A. Bendahmane, C. Robaglia, and C. Caranta. 2002. A natural recessive resistance gene against potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E (elF4E). Plant Journal 32: 1067–1075.

    CAS  Article  Google Scholar 

  29. Ruffel, S., J.L. Gallois, M.L. Lesage, and C. Caranta. 2005. The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene. Molecular Genetics and Genomics 274: 346–353.

    CAS  Article  Google Scholar 

  30. Sanfaçon, H. 2015. Plant translation factors and virus resistance. Viruses 7: 3392–3419.

    Article  Google Scholar 

  31. Truniger, V., and M.A. Aranda. 2009. Recessive resistance to plant viruses. Advances in Virus Research 75: 119–159.

    CAS  Article  Google Scholar 

  32. Wang, A., and S. Krishnaswamy. 2012. Eukaryotic translation initiation factor 4E-mediated recessive resistance to plant viruses and its utility in crop improvement. Molecular Plant Pathology 13: 795–803.

    CAS  Article  Google Scholar 

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Acknowledgements

This work was supported by the Michigan Potato Industry Commission.

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Affiliations

  1. Department of Plant, Soil and Microbial Sciences, Michigan State University, 1066 Bogue Street, East Lansing, MI, 48824, USA

    Chen Zhang, Kelly A. Zarka, Daniel G. Zarka & David S. Douches

  2. USDA-Agricultural Research Service, 1693 S 2700 W., Aberdeen, ID, 83210, USA

    Jonathan L. Whitworth

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  1. Chen Zhang
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  2. Kelly A. Zarka
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  5. David S. Douches
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Correspondence to David S. Douches.

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Zhang, C., Zarka, K.A., Zarka, D.G. et al. Expression of the Tomato pot-1 Gene Confers Potato Virus Y (PVY) Resistance in Susceptible Potato Varieties. Am. J. Potato Res. 98, 42–50 (2021). https://doi.org/10.1007/s12230-020-09815-y

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Keywords

  • Potato virus Y
  • Pot-1
  • Recessive resistance
  • eIF4E
  • Copy number variation