Skip to main content

Advertisement

Springer Nature Link
Log in

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

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Baulcombe DC, Chapman S, Santa-Cruz S (1995) Jellyfish green fluorescent protein as a reporter for virus infections. Plant J 7:1045–1053

    Article  PubMed  CAS  Google Scholar 

  • Bonierbale MW, Plaisted RL, Tanksley SD (1988) RFLP maps based on a common set of clones reveal modes of chromosomal evolution in potato and tomato. Genetics 120:1095–1103

    PubMed  Google Scholar 

  • Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphism. Am J Hum Genet 32:314–331

    PubMed  CAS  Google Scholar 

  • Browning KS (1996) the plant translational apparatus. Plant Mol Biol 32:107–143

    Article  PubMed  CAS  Google Scholar 

  • Diaz-Pendon JA, Truniger V, Nieto C, Garcia-Mas J, Bendahmane A, Aranda MA (2004) Advances in understanding recessive resistance to plant viruses. Mol Plant Pathol 5:223–233

    Article  CAS  Google Scholar 

  • Doganlar S, Frary A, Daunay MC, Lester RN, Tanksley SD (2002a) A comparative genetic linkage map of eggplant (Solanum melongena) and its implications for genome evolution in the Solanaceae. Genetics 161:1697–1711

    PubMed  CAS  Google Scholar 

  • Doganlar S, Frary A, Daunay MC, Lester RN, Tanksley SD (2002b) Conservation of gene function in the Solanaceae as revealed by comparative mapping of domestication traits in eggplant. Genetics 161:1713–1726

    PubMed  CAS  Google Scholar 

  • Duprat A, Caranta C, Revers F, Menand B, Browning KS, Robaglia C (2002) The Arabidopsis eukaryotic initiation factor (iso)4E is dispensable for plant growth but required for susceptibility to potyviruses. Plant J 32:927–934

    Article  PubMed  CAS  Google Scholar 

  • Eshed Y, Zamir D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141:1147–1162

    PubMed  CAS  Google Scholar 

  • Frary A, Doganlar S, Daunay MC, Tanksley SD (2003) QTL analysis of morphological traits in eggplant and implications for conservation of gene function during evolution of solanaceous species. Theor Appl Genet 107:359–370

    Article  PubMed  CAS  Google Scholar 

  • Gao Z, Johansen E, Eyers S, Thomas CL, Ellis THN, 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 

  • Grube RC, Radwanski ER, Jahn M (2000) Comparative genetics of disease resistance within the Solanaceae. Genetics 155:873–887

    PubMed  CAS  Google Scholar 

  • Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-Pdb Viewer: an environment for comparative protein modelling. Electrophoresis 18:2714–2723

    Article  PubMed  CAS  Google Scholar 

  • Lagercrantz U, Putterill J, Coupland G, Lydiate D (1996) Comparative mapping in Arabidopsis and Brassica, fine-scale genome colinearity and congruence of genes controlling flowering time. Plant J 9:13–20

    Article  PubMed  CAS  Google Scholar 

  • Lefebvre V, Pflieger S, Thabuis A, Caranta C, Blattes A, Chauvet JC, Daubèze AM, Palloix A (2002) Toward the saturation of the linkage map of pepper by alignment of 3 intraspecific maps including known-function genes. Genome 45:839–854

    Article  PubMed  CAS  Google Scholar 

  • Léonard S, Plante D, Wittman S, Daigneault N, Fortin MG, Laliberté JF (2000) Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. J Virol 74:7730–7737

    Article  PubMed  Google Scholar 

  • Liu YS, Zamir D (1999) Second generation L. pennellii introgression lines and the concept of bin mapping. Tomato Genet Coop Rep 49:26–30

    Google Scholar 

  • Livingstone KD, Lackney VK, Blauth JR, van Wijk R, Jahn MK (1999) Genome mapping in Capsicum and the evolution of genome structure in the Solanaceae. Genetics 152:1183–1202

    PubMed  CAS  Google Scholar 

  • Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK (1997) Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell 89:951–961

    Article  PubMed  CAS  Google Scholar 

  • Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK (1999) Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol Cell 3:707–716

    Article  PubMed  CAS  Google Scholar 

  • Moreau P, Thoquet P, Laterrot H, Moretti A, Olivier J, Grimsley NH (1997) A locus, Itm, controlling the development of intumescences, is present on chromosome 7. Tomato Genet Coop Rep 47:15–16

    Google Scholar 

  • Moury B, Morel C, Johansen E, Guilbaud L, Souche S, Ayme V, Caranta C, Palloix A, Jacquemond M (2004) Mutations in Potato virus Y genome-linked protein determine virulence toward recessive resistances in Capsicum annuum and Lycopersicon hirsutum. Mol Plant-Microbe Interact 17:322–329

    Article  PubMed  Google Scholar 

  • Neff MN, Turk E, Kalishman M (2002) Web-based primer design for single nucleotide polymorphism analysis. Trends Genet 18:613–615

    Article  PubMed  CAS  Google Scholar 

  • Nicaise V, German-Retana S, Sanjuan 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 

  • Parrella G, Ruffel S, Moretti A, Morel C, Palloix A, Caranta C (2002) Recessive resistance genes against potyviruses are localized in collinear genomic regions of the tomato (Lycopersicon spp.) and pepper (Capsicum spp.) genomes. Theor Appl Genet 105:855–861

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Burrow MD, Draye X, Elsik CG, Jiang CX, Katsar CS, Lan TH, Lin YR, Ming R, Wright RJ (2000) Comparative genomics of plant chromosomes. Plant Cell 12:1523–1540

    Article  PubMed  CAS  Google Scholar 

  • Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) ’Green revolution’ genes encode mutant gibberelin response modulators. Nature 400:256–261

    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, Caranta C, Palloix A, Lefebvre V, Caboche M, Bendahmane A (2004) Structural analysis of the eukaryotic initiation factor 4E gene controlling potyvirus resistance in pepper: exploitation of a BAC library. Gene 338:209–216

    Article  PubMed  CAS  Google Scholar 

  • Schaad MC, Anderberg RJ, Carrington JC (2000) Strain-specific interaction of the tobacco etch virus NIa protein with the translation initiation factor eIF4E in the yeast two-hybrid system. Virology 273:300–306

    Article  PubMed  CAS  Google Scholar 

  • Tanksley SD, et al (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160

    PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Thorup TA, Tanyolac B, Livingstone KD, Popovsky S, Paran I, Jahn M (2000) Candidate gene analysis of organ pigmentation loci in the Solanaceae. Proc Natl Acad Sci USA 97:11192–11197

    Article  PubMed  CAS  Google Scholar 

  • Wittmann S, Chatel H, Fortin MG, Laliberté JF (1997) Interaction of the viral protein genome linked of turnip mosaic potyvirus with the translational eukaryotic initiation factor (iso)4E of Arabidopsis thaliana using the yeast two-hybrid system. Virology 234:84–92

    Article  PubMed  CAS  Google Scholar 

Download references

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

Author information

Authors and Affiliations

  1. Genetics and Breeding of Fruits and Vegetables, Institut National de la Recherche Agronomique (INRA), Dom. St Maurice, BP94, 84143, Montfavet Cedex, France

    S. Ruffel, J. L. Gallois, M. L. Lesage & C. Caranta

Authors
  1. S. Ruffel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. L. Gallois
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. L. Lesage
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Caranta
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. Caranta.

Additional information

Communicated by M.-A. Grandbastien

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-005-0003-x

Keywords

Search

Navigation