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The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene

Abstract

The translation initiation factor 4E (eIF4E) has been implicated in naturally occurring resistance to Potato virus Y (PVY) determined by the pvr2 locus in pepper (Capsicum annuum). Here, the molecular basis of the recessive resistance to PVY and Tobacco etch virus (TEV) controlled by the pot-1 locus in tomato (Lycopersicon esculentum; now Solanum lycopersicum) was investigated. On the basis of genetic mapping data that indicated that pot-1 and pvr2 are located in syntenic regions of the tomato and pepper genomes, the possible involvement of eIF4E in pot-1-mediated resistance was assessed. Genetic mapping of members of the eIF4E multigenic family in tomato introgression lines revealed that an eIF4E locus indeed maps in the same genomic region as pot-1. By comparing eIF4E coding sequences between resistant and susceptible Lycopersicon genotypes, a small number of polymorphisms that co-segregate with the pot-1 locus were identified, suggesting that this gene could be involved in resistance to potyviruses. Functional complementation experiments using Potato virus X-mediated transient expression of eIF4E from a susceptible genotype in a resistant pepper genotype confirmed that a small number of amino acid substitutions in the eIF4E protein indeed account for resistance/susceptibility to both the PVY and TEV, and consequently that pot-1 and pvr2 are orthologues. Taken together, these results support the role of this eIF4E gene as a key component of recessive resistance to potyviruses, and validate the comparative genomic approach for the molecular characterization of recessive resistance genes.

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Acknowledgements

We thank Rebecca Stevens, Ken Richards, Thierry Candresse, Christophe Robaglia, Olivier Le Gall and Benoit Moury for critical comments on the manuscript. This research was supported by a GENOPLANTE grant (CI-2001-005), a doctoral fellowship from the Provence-Alpes Côte d’Azur region to S. Ruffel and a post-doctoral fellowship from the Ministère de la Recherche to J. L. Gallois. Experiments were carried out in compliance with current French guidelines concerning GMOs

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Correspondence to C. Caranta.

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Communicated by M.-A. Grandbastien

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Ruffel, S., Gallois, J.L., Lesage, M.L. et al. The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene. Mol Genet Genomics 274, 346–353 (2005). https://doi.org/10.1007/s00438-005-0003-x

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Keywords

  • Solanum lycopersicum
  • Eukaryotic translation initiation factor 4E (eIF4E)
  • Comparative mapping
  • Potato virus Y
  • Tobacco etch virus