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
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
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
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
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
Garbarino JE, Oosumi T, Belknap WR (1995) Isolation of a polyubiquitin promoter and its expression in transgenic potato plants. Plant Physiol 109:1371–1378
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
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
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
Ibiza VP, Cañizares J, Nuez F (2010) EcoTILLING in Capsicum species: searching for new virus resistances. BMC Genomics 11:631
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
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
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
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
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
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
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
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
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
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
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
Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11:40–45
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
Rommens CM, Bougri O, Yan H, Humara JM, Owen J, Swords K, Ye J (2005) Plant-derived transfer DNAs. Plant Physiol 139:1338–1349
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
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
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
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
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
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
Truniger V, Aranda MA (2009) Recessive resistance to plant viruses. Adv Virus Res 75:119–159
Yan H, Chretien R, Ye J, Rommens CM (2006) New construct approaches for efficient gene silencing in plants. Plant Phys 141:1508–1518
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
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We thank Dr. Hua Yan, Heather Holloway, Matthew Burns, and Christie Caplinger for excellent technical support.
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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)
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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