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Overexpression of the wild potato eIF4E-1 variant Eva1 elicits Potato virus Y resistance in plants silenced for native eIF4E-1

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Abstract

Potato virus Y (PVY) is the most important viral pathogen of cultivated potato (Solanum tuberosum) from a commercial perspective, causing severe losses in both tuber quality and yield worldwide. Specific accessions of wild potato species exhibit resistance against PVY but efforts to transfer the trait to cultivated material have not yielded widely adopted varieties. Because amino acid substitutions at specific domains of host factor eIF4E-1 often confer resistance to various crops, we sequenced the associated genes expressed in wild potato plants. A novel eIF4E-1 variant, designated here as Eva1, was identified in S. chacoense, S. demissum, and S. etuberosum. The protein contains amino acid substitutions at ten different positions when compared to its cultivated potato (S. tuberosum) homolog. In the yeast two-hybrid system, Eva1 failed to bind VPg, a viral protein required for infectivity. Overexpression of the associated cDNA conferred PVY resistance to transgenic potato plants silenced for the native eIF4E-1 gene. Because the gene sources of Eva1 are sexually compatible with potato, the molecular strategies described can be employed to develop ‘intragenic’ potato cultivars.

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References

  • Arif M, Azhar U, Arshad M, Zafar Y, Mansoor S, Asad S (2011) Engineering broad-spectrum resistance against RNA viruses in potato. Transgenic Res. doi:10.1007/S11248-011-9533-7

  • Ashby JA, Stevenson CE, Jarvis GE, Lawson DM, Maule AJ (2011) Structure-based mutational analysis of eIF4E in relation to sbm1 resistance to pea seed-borne mosaic virus in pea. PLoS One 6:e15873

    Article  PubMed  CAS  Google Scholar 

  • Caranta C, Ruffel S, Bendahmane A, Palloix A, Robaglia C (2011) eIF4E gene mutations and potyvirus resistance. US Patent 7919677

  • Cavatorta J, Perez KW, Gray SM, Van Eck J, Yeam I, Jahn M (2011) Engineering virus resistance using a modified potato gene. Plant Biotechnol J 9:1014–1021

    Article  PubMed  CAS  Google Scholar 

  • Ellis P, Stace-Smith R, Bowler G, MacKenzie DJ (1996) Production of monoclonal antibodies for detection and identification of strains of Potato virus Y. Can J Plant Pathol 18:64–70

    Article  Google Scholar 

  • Gao Z, Johansen E, Eyers S, Thomas CL, Noel Ellis TH, Maule AJ (2004) The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J 40:376–385

    Article  PubMed  CAS  Google Scholar 

  • Garbarino JE, Belknap WR (1994) Isolation of a ubiquitin-ribosomal protein gene (ubi3) from potato and expression of its promoter in transgenic plants. Plant Mol Biol 24:119–127

    Article  PubMed  CAS  Google Scholar 

  • Garbarino JE, Oosumi T, Belknap WR (1995) Isolation of a polyubiquitin promoter and its expression in transgenic potato plants. Plant Physiol 109:1371–1378

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Hermsen JGT (1994) Introgression of genes from wild species, including molecular and cellular approaches. In: Bradshaw JE, Mackay GR (eds) Potato genetics. CAB International, Oxon, pp 515–538

    Google Scholar 

  • Horvath J, Kolber M, Wolf I (1988) Reactions of wild Solanum species to Potato virus X and Potato virus Y. Acta Phytop Ent Hung 23:465–470

    Google Scholar 

  • Ibiza VP, Cañizares J, Nuez F (2010) EcoTILLING in Capsicum species: searching for new virus resistances. BMC Genomics 11:631

    Article  PubMed  Google Scholar 

  • Jahn M, Kang BC (2010) Recessive plant viral resistance results from mutations in translation initiation factor eIF4E. US Patent 7,772,462

  • Jenner CE, Nellist CF, Barker GC, Walsh JA (2010) Turnip mosaic virus (TuMV) is able to use alleles of both eIF4E and eIF(iso)4E from multiple loci of the diploid Brassica rapa. Mol Plant Microbe Interact 23:1498–1505

    Article  PubMed  CAS  Google Scholar 

  • Kang BC, Yeam I, Frantz JD, Murphy JF, Jahn MM (2005) The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant J 42:392–405

    Article  PubMed  CAS  Google Scholar 

  • Kang BC, Yeam I, Li H, Perez KW, Jahn MM (2007) Ectopic expression of a recessive resistance gene generates dominant potyvirus resistance in plants. Plant Biotechnol J 5:526–536

    Article  PubMed  CAS  Google Scholar 

  • Kanyuka K, Druka A, Caldwell DG, Tymon A, McCallum N, Waugh R, Adams MJ (2005) Evidence that the recessive Bymovirus resistance locus rym4 in barley corresponds to the eukaryotic translation initiation factor 4E gene. Mol Plant Pathol 6:449–458

    Article  PubMed  CAS  Google Scholar 

  • Lawson C, Kaniewski W, Haley L, Rozman R, Newell C, Sanders P, Tumer NE (1990) Engineering resistance to mixed virus infection in a commercial potato cultivar: resistance to Potato virus X and Potato virus Y in transgenic Russet Burbank. Biotechnol J 8:127–134

    Article  CAS  Google Scholar 

  • Naderpour M, Lund OS, Larsen R, Johansen E (2010) Potyviral resistance derived from cultivars of Phaseolus vulgaris carrying bc-3 is associated with the homozygotic presence of a mutated eIF4E allele. Mol Plant Pathol 11:255–263

    Article  PubMed  CAS  Google Scholar 

  • Nicaise V, German-Retana S, Sanjuán R, Dubrana MP, 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 Physiol 132:1272–1282

    Article  PubMed  CAS  Google Scholar 

  • Nicot N, Hausman JF, Hoffmann L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 56:2907–2914

    Article  PubMed  CAS  Google Scholar 

  • Nieto C, Morales M, Orjeda G, Clepet C, Monfort A, Sturbois B, Puigdomènech P, Pitrat M, Caboche M, Dogimont C, Garcia-Mas J, Aranda MA, Bendahmane A (2006) An eIF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon. Plant J 48:452–462

    Article  PubMed  CAS  Google Scholar 

  • Nieto C, Piron F, Dalmais M, Marco CF, Moriones E, Gómez-Guillamón ML, Truniger V, Gómez P, Garcia-Mas J, Aranda MA, Bendahmane A (2007) EcoTILLING for the identification of allelic variants of melon eIF4E, a factor that controls virus susceptibility. BMC Plant Biol 7:34–42

    Article  PubMed  Google Scholar 

  • Piron F, Nicolaï M, Minoïa S, Piednoir E, Moretti A, Salgues A, Zamir D, Caranta C, Bendahmane A (2010) An induced mutation in tomato eIF4E leads to immunity to two potyviruses. PLoS One 5:e11313

    Article  PubMed  Google Scholar 

  • Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11:40–45

    Article  PubMed  CAS  Google Scholar 

  • Rommens CM, Humara JM, Ye J, Yan H, Richael C, Zhang L, Perry R, Swords K (2004) Crop improvement through modification of the plant’s own genome. Plant Physiol 135:421–431

    Article  PubMed  CAS  Google Scholar 

  • Rommens CM, Bougri O, Yan H, Humara JM, Owen J, Swords K, Ye J (2005) Plant-derived transfer DNAs. Plant Physiol 139:1338–1349

    Article  PubMed  CAS  Google Scholar 

  • Rommens CM, Haring MA, Swords K, Davies HV, Belknap WR (2007) The intragenic approach as a new extension to traditional plant breeding. Trends Plant Sci 12:397–403

    Article  PubMed  CAS  Google Scholar 

  • Rubio M, Nicolaï M, Caranta C, Palloix A (2009) Allele mining in the pepper gene pool provided new complementation effects between pvr2-eIF4E and pvr6-eIF(iso)4E alleles for resistance to Pepper veinal mottle virus. J Gen Virol 90:2808–2814

    Article  PubMed  CAS  Google Scholar 

  • Ruffel S, Dussault MH, Palloix A, Moury B, Bendahmane A, Robaglia C, Caranta C (2002) A natural recessive resistance gene against Potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E (eIF4E). Plant J 32:1067–1075

    Article  PubMed  CAS  Google Scholar 

  • Ruffel S, Gallois JL, Lesage ML, Caranta C (2005) The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene. Mol Genet Genomics 274:346–353

    Article  PubMed  CAS  Google Scholar 

  • Ruffel S, Gallois JL, 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. J Gen Virol 87:2089–2098

    Article  PubMed  CAS  Google Scholar 

  • Stein N, Perovic D, Kumlehn J, Pellio B, Stracke S, Streng S, Ordon F, Graner A (2005) The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). Plant J 42:912–922

    Article  PubMed  CAS  Google Scholar 

  • Truniger V, Aranda MA (2009) Recessive resistance to plant viruses. Adv Virus Res 75:119–159

    Article  PubMed  CAS  Google Scholar 

  • Yan H, Chretien R, Ye J, Rommens CM (2006) New construct approaches for efficient gene silencing in plants. Plant Phys 141:1508–1518

    Google Scholar 

  • Yoshii M, Nishikiori M, Tomita K, Yoshioka N, Kozuka R, Naito S, Ishikawa M (2004) The Arabidopsis cucumovirus multiplication 1 and 2 loci encode translation initiation factors 4E and 4G. J Virol 78:6102–6111

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr. Hua Yan, Heather Holloway, Matthew Burns, and Christie Caplinger for excellent technical support.

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Correspondence to Caius M. Rommens.

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11248_2011_9576_MOESM1_ESM.ppt

Supplementary Figure 1. Symptom development following PVYNTN infection. Leaves shown are from a mock-infected control plant (left) and a plant that had been infected two weeks before (right). (PPT 1560 kb)

11248_2011_9576_MOESM2_ESM.ppt

Supplementary Figure 2. SteIF4E-1 transcript levels in silencing transgenic potato. Leaf RNA from the wild type Russet Burbank (wt), transgenic plants carrying the empty vector control (vc), and plants from the transgenic lines 1895/1-13 were hybridized with a SteIF4E-1-derived probe. Ethidium bromide-stained ribosomal RNA was used as a loading control. (PPT 563 kb)

11248_2011_9576_MOESM3_ESM.docx

Supplementary Figure 3. Alignment of resistance-associate eIF4E proteins. Amino acid differences with the homologous proteins of susceptible genotypes are highlighted in gray. (DOCX 18 kb)

Supplementary material 4 (PDF 32 kb)

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Duan, H., Richael, C. & Rommens, C.M. Overexpression of the wild potato eIF4E-1 variant Eva1 elicits Potato virus Y resistance in plants silenced for native eIF4E-1 . Transgenic Res 21, 929–938 (2012). https://doi.org/10.1007/s11248-011-9576-9

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  • DOI: https://doi.org/10.1007/s11248-011-9576-9

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