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American Journal of Potato Research

, Volume 93, Issue 1, pp 64–71 | Cite as

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

  • Erica Arcibal
  • Kaitlin Morey Gold
  • Stephanie Flaherty
  • Jiming Jiang
  • Molly Jahn
  • Aurélie M. Rakotondrafara
Article
  • 397 Downloads

Abstract

Potato Virus Y (PVY) is one of the most important pathogens affecting potato production worldwide. Here we tested the efficacy of engineered resistance against PVY in two popular susceptible potato varieties, Russet Norkotah and Atlantic. This resistance is based on the expression of a modified potato eIF4E gene containing mutations homologous to those in the recessive resistant allelic variant found in pepper. The expression of this eIF4E variant conferred differential resistance responses against three prevalent PVY strains including PVYO, PVYN:O and PVYNTN in the five tested transgenic lines. When resistance was established, the virus was not detectable in the inoculated leaves, the newly emerged leaves, nor in the sprouted tubers. Some strains were restrained to a low but detectable level in some of the potato lines. Crosses between transformed and wild type lines demonstrated that the engineered resistance gene was inherited in a dominant manner.

Keywords

Potyviridae pvr12 Recessive resistance Dominant inheritance eIF4E Potato virus Y 

Resumen

El virus Y de la papa (PVY) es uno de los patógenos más importantes que afectan la producción de la papa a nivel mundial. Aquí probamos la eficacia de resistencia asistida contra PVY en dos variedades susceptibles populares de papa, Russet Norkotah y Atlantic. Esta resistencia se basa en la expresión de un gen modificado de papa, eIF4E, que contiene mutaciones homólogas a aquellas de la variante alélica resistente recesiva encontrada en pimiento. La expresión de esta variante eIF4E confiere respuestas de resistencia diferencial contra tres variantes prevalentes de PVY incluyendo PVYO, PVYN:O y PVYNTN en las cinco líneas transgénicas probadas. Cuando se estableció la resistencia, el virus no fue detectable en las hojas inoculadas, en las nuevas hojas emergidas, ni en los tubérculos brotados. Algunas variantes se restringieron a un nivel bajo, pero detectable, en algunas de las líneas de papa. Las cruzas entre líneas transformadas y las de tipo silvestre demostraron que el gen de la resistencia asistida era heredable de manera dominante.

Notes

Acknowledgments

We thank Dr. Dennis Halterman for his generous support and Dr. Amy Charkowski for inoculum and critical comments on the manuscript.

This research was supported by the Wisconsin Potato Industry Board (MSN170065 and MSN180863 to AR) and a Hatch Act Formula Fund to J.J.

Supplementary material

12230_2015_9489_MOESM1_ESM.xlsx (45 kb)
ESM 1 (XLSX 45 kb)

References

  1. Ayme, V., S. Souche, C. Caranta, M. Jacquemond, J. Chadoeuf, A. Palloix, and B. Moury. 2006. Different mutations in the genome-linked protein VPg of potato virus Y confer virulence on the pvr2(3) resistance in pepper. Molecular Plant-Microbe Interactions 19: 557–563.CrossRefPubMedGoogle Scholar
  2. Bhaskar, P.B., J.A. Raasch, L.C. Kramer, P. Neumann, S.M. Wielgus, S. Austin-Phillips, and J. Jiang. 2008. Sgt1, but not Rar1, is essential for the RB-mediated broad-spectrum resistance to potato late blight. BMC Plant Biology 8: 8.PubMedCentralCrossRefPubMedGoogle 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.CrossRefPubMedGoogle Scholar
  4. Chandler, J.W., and W. Werr. 2003. When negative is positive in functional genomics. Trends Plant Science 8: 279–285.CrossRefGoogle Scholar
  5. Charron, C., M. Nicolai, J.L. Gallois, C. Robaglia, B. Moury, A. Palloix, and C. Caranta. 2008. Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant Journal 54: 56–68.CrossRefPubMedGoogle Scholar
  6. Crosslin, J.M., K.C. Hamm, R.E. Thornton, C.R. Brown, P. Corsini, J. Shiel, and P.H. Berger. 2002. First report of the necrotic strain of potato virus Y (PVYN) on potatoes in the northwestern United States. Plant Disease 86: 1177.CrossRefGoogle Scholar
  7. Draper, M.D., J.S. Pasche, and N.C. Gudmestand. 2002. Factors influencing PVY development and disease expression in three potato cultivars. American Journal of Potato Research 79: 155–165.CrossRefGoogle Scholar
  8. 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.CrossRefPubMedGoogle Scholar
  9. Frost, K.E., R.L. Groves, and A.O. Charkowski. 2013. Integrated control of potato pathogens through seed potato certification and provision of clean seed potatoes. Plant Disease 97: 1268–1280.CrossRefGoogle Scholar
  10. Gray, S.M., J.L. Solke De Boer, A.V. Karasev, J. Whitworth, R. Singh, A. Boucher, and X. Huimin. 2010. Potato virus Y: an evolving concern for potato crops in the United States and Canada. Plant Disease 94: 1384–1397.CrossRefGoogle Scholar
  11. Kang, B.C., 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.CrossRefPubMedGoogle Scholar
  12. Karasev, A.V., and S.M. Gray. 2013. Continuous and emerging challenges of Potato virus Y in potato. Annual Review of Phytopathololgy 51: 571–586.CrossRefGoogle Scholar
  13. Karasev, A.V., X. Hu, C.J. Brown, C. Kerlan, O.V. Nikolaeva, J.M. Crosslin, and S.M. Gray. 2011. Genetic diversity of the ordinary strain of Potato Virus Y (PVY) and origin of recombinant PVY strains. Phytopathology 101: 778–785.PubMedCentralCrossRefPubMedGoogle Scholar
  14. Leonard, S., D. Plante, S. Wittmann, N. Daigneault, M.G. Fortin, and J.F. Laliberte. 2000. Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. Journal of Virology 74: 7730–7737.PubMedCentralCrossRefPubMedGoogle Scholar
  15. McDonald, J.G., and R.P. Singh. 1996. Host range, symptomology, and serology of isolates of Potato Virus Y (PVY) that share properties with both the PVYN and PVYO strain groups. American Journal of Potato Research 73: 309–315.CrossRefGoogle Scholar
  16. Moury, B., C. Morel, E. Johansen, L. Guilbaud, S. Souche, V. Ayme, C. Caranta, A. Palloix, and M. Jacquemond. 2004. Mutations in potato virus Y genome-linked protein determine virulence toward recessive resistances in Capsicum annuum and Lycopersicon hirsutum. Molecular Plant-Microbe Interactions 17: 322–329.CrossRefPubMedGoogle Scholar
  17. Moury, B., C. Charron, B. Janzac, V. Simon, J.L. Gallois, A. Palloix, and C. Caranta. 2014. Evolution of plant eukaryotic initiation factor 4E (eIF4E) and potyvirus genome-linked protein (VPg): a game of mirrors impacting resistance spectrum and durability. Infection, Genetics and Evolution 27: 472–480.CrossRefPubMedGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. Porebski, S., L. Grant Bailey, and B.R. Baum. 1997. Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Molecular Biology Reporter 15: 8–15.CrossRefGoogle Scholar
  20. 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.CrossRefPubMedGoogle Scholar
  21. Robaglia, C., and C. Caranta. 2006. Translation initiation factors: a weak link in plant RNA virus infection. Trends in Plant Science 11: 40–45.CrossRefPubMedGoogle Scholar
  22. Ruffel, S., M.H. 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 (eIF4E). Plant Journal 32: 1067–1075.CrossRefPubMedGoogle Scholar
  23. Song, J., J.M. Bradeen, S.K. Naess, J.A. Raasch, S.M. Wielgus, G.T. Haberlach, J. Liu, H. Kuang, S. Austin-Phillips, C.R. Buell, J.P. Helgeson, and J. Jiang. 2003. Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proceedings of the National Academy of Sciences 100: 9128–9133.CrossRefGoogle Scholar
  24. Truniger, V., and M.A. Aranda. 2009. Recessive resistance to plant viruses. Advances in Virus Research 75: 119–159.CrossRefPubMedGoogle Scholar
  25. 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.CrossRefPubMedGoogle Scholar

Copyright information

© The Potato Association of America 2015

Authors and Affiliations

  • Erica Arcibal
    • 1
  • Kaitlin Morey Gold
    • 1
  • Stephanie Flaherty
    • 2
  • Jiming Jiang
    • 2
  • Molly Jahn
    • 3
  • Aurélie M. Rakotondrafara
    • 1
  1. 1.Department of Plant PathologyUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.Department of HorticultureUniversity of Wisconsin-MadisonMadisonUSA
  3. 3.Department of AgronomyUniversity of Wisconsin-MadisonMadisonUSA

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