Skip to main content
SpringerLink
Log in

A Eukaryotic Translation Initiation Factor 4E (eIF4E) is Responsible for the “va” Tobacco Recessive Resistance to Potyviruses

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Potato virus Y (PVY), the type member of the genus Potyvirus, is transmitted by aphids and can cause severe damage in several solanaceous family crops. In Nicotiana tabacum, a large genome deletion conferring resistance to PVY, the va gene, is commonly used. This resistance is unfortunately associated with lower tobacco quality parameters, potentially due to the presence of several other important genes in the deleted region. In the present study, we have used next-generation sequencing to analyze the transcriptome of a dozen of tobacco F7 recombinant inbred lines (RILs) segregating for PVY resistance. After comparison with a reference transcriptome, genes differentially expressed between resistant and susceptible plants were identified. About 30 candidate sequences were selected, including a sequence annotated as encoding an eukaryotic translation initiation factor 4E (eIF4E), which was strongly expressed in susceptible plants but not in resistant ones. Other differentially expressed candidates are mostly related to photosynthesis. A complete correlation between susceptibility and expression of this eIF4E sequence was confirmed by amplification in 91 F8 RILs and in a segregating F2 population. The gene was mapped on chromosome 21 of the tobacco genetic map and corresponds to an eIF4E isoform derived from the N. sylvestris parent of tobacco. Final confirmation of the identification of the va gene came from the analysis of two tobacco lines with missense mutations in the eIF4E gene and which correspondingly showed resistance to PVY infection. Screening of a large collection of tobacco accessions revealed a strong correlation between the status of this eIF4 gene and PVY resistance, but the identification of a few resistant accessions with an apparently intact gene suggests the possible existence of alternative resistance sources. The identification of the va gene and of molecular markers linked to it or to the large deletion associated with it opens the way to breeding efforts aimed at breaking the linkage drag associated with this valuable resistance gene.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Acosta-Leal R, Xiong Z (2008) Complementary functions of two recessive R-genes determine resistance durability of tobacco ‘Virgin A Mutant’ (VAM) to Potato virus Y. Virology 379:275–283

    Article  CAS  PubMed  Google Scholar 

  • Acosta-Leal R, Xiong Z (2013) Intrahost mechanisms governing emergence of resistance-breaking variants of potato virus Y. Virology 437:39–47

    Article  CAS  PubMed  Google Scholar 

  • Athow KL, Laviolette FA, Wilcox JR, Abney TS (1987) Registration of “TN86” burley tobacco. Crop Sci 27:365–366

    Article  Google Scholar 

  • Bindler G, Plieske J, Bakaher N, Gunduz I, Ivanov N, Van der Hoeven R, Ganal M, Donini P (2011) A high density genetic map of tobacco (Nicotiana tabacum L.) obtained from large scale microsatellite marker development. Theor Appl Genet 123:219–230

    Article  PubMed Central  PubMed  Google Scholar 

  • Blancard D, Ano G, Cailleteau B (1995) Etude du pouvoir pathogène d’isolats de PVY sur Tabac: proposition d’une classification intégrant la résistance à la nécrose. Annales du Tabac, Seita 2(27):43–50

    Google Scholar 

  • Burk LG, Chaplin JF, Gooding GV, Powell NT (1979) Quantity production of anther-derived haploids from a multiple disease resistant tobacco hybrid. I. Frequency of plants with resistance or susceptibility to tobacco mosaic virus (TMV), potato virus Y (PVY), and root knot (RK). Euphytica 28:201–208

    Article  Google Scholar 

  • Clarkson JJ, Lim KY, Kovarik A, Chase MW, Knapp S, Leitch AR (2005) Long-term genome diploidization in allopolyploid Nicotiana section Repandae (Solanaceae). New Phytol 168:241–252

    Article  CAS  PubMed  Google Scholar 

  • Conesa A, Götz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  PubMed  Google Scholar 

  • Decroocq V, Sicard O, Alamillo JM, Lansac M, Eyquard JP, García JA, Candresse T, Le Gall O, Revers F (2006) Multiple resistance traits control Plum pox virus infection in Arabidopsis thaliana. Mol Plant Microbe Interact 19:541–549

    Article  CAS  PubMed  Google Scholar 

  • Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:W465-469. Epub 2008 Apr 19

  • 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  PubMed  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  CAS  PubMed  Google Scholar 

  • Edwards KD, Bombarely A, Story GW, Allen F, Mueller LA, Coates SA, Jones L (2010) TobEA: an atlas of tobacco gene expression from seed to senescence. BMC Genomics 11:142

    Article  PubMed Central  PubMed  Google Scholar 

  • Gupta S, Shi X, Lindquist IE, Devitt N, Mudge J, Rashotte AM (2013) Transcriptome profiling of cytokinin and auxin regulation in tomato root. J Exp Bot 64:695–704

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gupton CL, Burk LG (1973) Location of the factor for resistance to potato virus Y in tobacco. J Hered 64:289–290

    CAS  PubMed  Google Scholar 

  • Hasegawa K, Yukawa Y, Sugita M, Sugiura M (2002) Organization and transcription of the gene family encoding chlorophyll a/b-binding proteins in Nicotiana sylvestris. Gene 289:161–168

    Article  CAS  PubMed  Google Scholar 

  • Hwang J, Li J, Liu WY, An SJ, Cho H, Her NH, Yeam I, Kim D, Kang BC (2009) Double mutations in eIF4E and eIFiso4E confer recessive resistance to Chilli veinal mottle virus in pepper. Mol Cells 27:329–336

    Article  CAS  PubMed  Google Scholar 

  • Julio E, Verrier J-L, Dorlhac de Borne F (2006) Development of SCAR markers linked to three disease resistances based on AFLP within Nicotiana tabacum L. Theor Appl Genet 112:335–346

    Article  CAS  PubMed  Google Scholar 

  • Julio E, Laporte F, Reis S, Rothan C, Dorlhac de Borne F (2008) Reducing the content of nornicotine in tobacco via targeted mutation breeding. Mol Breed 21:369–381

    Article  CAS  Google Scholar 

  • Jung J, Yeam I (2013) Exploring natural variations in eIF4E and screening for potyviral resistance in diverse Nicotiana species. Hort Environ Biotechnol 54:430–440

    Article  CAS  Google Scholar 

  • Koelle G (1961) Genetic analyse einer Y-virus (Rippenbraune) resistenten mutante der tabaksorte Virgin A. Zuchter 31:71–71

    Google Scholar 

  • Komari T, Kubo T, Sato M (1986) Inheritance of the low-duvatriendol trait in Nicotiana tabacum L. Tob Sci 30:159–162

    Google Scholar 

  • Lacroix C, Glais L, Kerlan C, Verrier JL, Jacquot E (2010) Biological characterization of French potato virus Y (PVY) isolates collected from PVY-susceptible or -resistant tobacco plants possessing the recessive resistance gene va. Plant Pathol 59:1133–1143

    Article  Google Scholar 

  • Lacroix C, Glais L, Verrier JL, Jacquot E (2011) Effect of passage of a potato virus Y isolate on a line of tobacco containing the recessive resistance gene va(2) on the development of isolates capable of overcoming alleles 0 and 2. Eur J Plant Pathol 130:259–269

    Article  CAS  Google Scholar 

  • Lellis AD, Kasschau KD, Whitham SA, Carrington JC (2002) Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr Biol 12:1046–1051

    Article  CAS  PubMed  Google Scholar 

  • Léonard S, Plante D, Wittmann 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 Central  PubMed  Google Scholar 

  • Lewis RS (2005) Transfer of resistance to potato virus Y (PVY) from Nicotiana africana to Nicotiana tabacum: possible influence of tissue culture on the rate of introgression. Theor Appl Genet 110:678–687

    Article  CAS  PubMed  Google Scholar 

  • Lewis RS (2007) Evaluation of Nicotiana tabacum genotypes possessing Nicotiana africana-derived genetic tolerance to potato virus Y. Crop Sci 47:1975–1984

    Article  Google Scholar 

  • Lim KY, Matyasek M, Kovarik A, Leitch AR (2004) Genome evolution in allotetraploid Nicotiana. Reports of the International Polyploidy Conference, London, UK, 27–30 April 2003

  • Lu J, Du ZX, Kong J, Chen LN, Qiu YH, Li GF, Meng XH, Zhu SF (2012) Transcriptome analysis of Nicotiana tabacum infected by cucumber mosaic virus during systemic symptom development. PLoS One 7(8):e43447

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martin F, Bovet L, Cordier A, Stanke M, Gunduz I, Peitsch MC, Ivanov NV (2012) Design of a tobacco exon array with application to investigate the differential cadmium accumulation property in two tobacco varieties. BMC Genomics 28(13):674

    Article  Google Scholar 

  • Masuta C, Nishimura M, Morishita H, Hataya T (1999) A single amino acid change in viral genome-associated protein of potato virus y correlates with resistance breaking in ‘virgin a mutant’ tobacco. Phytopathology 89:118–123

    Article  CAS  PubMed  Google Scholar 

  • Mazier M, Flamain F, Nicolaï M, Sarnette V, Caranta C (2011) Knock-down of both eIF4E1 and eIF4E2 genes confers broad-spectrum resistance against potyviruses in tomato. PLoS ONE 6(12):e29595

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McCallum CM, Comai L, Greene EA, Henikoff S (2000) Targeted screening for induced mutations. Nat Biotechnol 18:455–457

    Article  CAS  PubMed  Google Scholar 

  • Murad L, Lim KY, Christopodulou V, Matyasek R, Lichtenstein CP, Kovarik A, Leitch AR (2002) The origin of tobacco’s T genome is traced to a particular lineage within Nicotiana tomentosiformis (Solanaceae). Am J Bot 89:921–928

    Article  CAS  PubMed  Google Scholar 

  • Ng PC, Henikoff S (2003) SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res 31:3812–3814

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nicaise V (2006) Etude des facteurs cellulaires impliqués dans les interactions plante-virus : rôle du facteur d’initiation à la traduction 4E (eIF4E). Ph.D. thesis, UMR 1090, INRA-Université Bordeaux 2

  • 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 Central  CAS  PubMed  Google Scholar 

  • Nielsen MT, Jones GA, Collins GB (1982) Inheritance pattern for secreting and non secreting glandular trichomes in tobacco. Crop Sci 22:1051–1053

    Article  Google Scholar 

  • Noguchi S, Tajima T, Yamamoto Y, Ohno T, Kubo T (1999) Deletion of a large genomic segment in tobacco varieties that are resistant to potato virus Y (PVY). Mol Gen Genet 262:822–829

    Article  CAS  PubMed  Google Scholar 

  • Palloix A, Ayme V, Moury B (2009) Durability of plant major resistance genes to pathogens depends on the genetic background, experimental evidence and consequences for breeding strategies. New Phytol 183:190–199

    Article  CAS  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 25;5(6):e11313

    Article  Google Scholar 

  • Quenouille J, Montarry J, Palloix A, Moury B (2013) Farther, slower, stronger: how the plant genetic background protects a major resistance gene from breakdown. Mol Plant Patholology 14:109–118

    Article  CAS  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  CAS  PubMed  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  CAS  PubMed  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 Gen and Genomics 274:346–353

    Article  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  CAS  PubMed  Google Scholar 

  • Ruud KA, Kuhlow C, Goss DJ, Browning KS (1998) Identification and characterization of a novel cap-binding protein from Arabidopsis thaliana. J Biol Chem 273:10325–10330

    Article  CAS  PubMed  Google Scholar 

  • Sato M, Nakahara K, Yoshii M, Ishikawa M, Uyeda I (2005) Selective involvement of members of the eukaryotic initiation factor 4E family in the infection of Arabidopsis thaliana by potyviruses. FEBS Lett 579:1167–1171

    Article  CAS  PubMed  Google Scholar 

  • Scholthof KB, Adkins S, Czosnek H, Palukaitis P, Jacquot E, Hohn T, Hohn B, Saunders K, Candresse T, Ahlquist P, Hemenway C, Foster GD (2011) Top 10 plant viruses in molecular plant pathology. Mol Plant Pathol 12:938–954

    Article  CAS  PubMed  Google Scholar 

  • Sierro N, van Oeveren J, van Eijk MJ, Martin F, Stormo KE, Peitsch MC, Ivanov NV (2013) Whole genome profiling physical map and ancestral annotation of tobacco Hicks Broadleaf. Plant J 75:880–889

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Strickler SR, Bombarely A, Mueller LA (2012) Designing a transcriptome next-generation sequencing project for a nonmodel plant species. Am J Bot 99:257–266, Review

    Article  CAS  PubMed  Google Scholar 

  • Tajima T, Noguchi S, Tanoue W, Negishi H, Nakakawaji T, Ohno T (2002) Background selection using DNA markers in backcross breeding program for potato virus Y resistance of tobacco. Breed Sci 52:253–257

    Article  Google Scholar 

  • Till BJ, Reynolds SH, Greene EA et al (2003) Large-scale discovery of induced point mutations with high-throughput TILLING. Genome Res 13:524–530

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Van Ooijen JW, Vooririps RE (2001) JoinMap ® 3.0, software for the calculation of genetic linkage maps. In: Plant research international. Wageningen, Netherlands

    Google Scholar 

  • Verrier JL, Doroszewska T (2004) The “va” resistance to PVYN in Nicotiana tabacum: an assessment of the frequency of “va” breaking PVYN strains based on seven years of field survey on a worldwide basis. In: 12th European Association for Potato Research virology section meeting. Rennes, France

    Google Scholar 

  • Wang A, Krishnaswamy S (2012) Eukaryotic translation initiation factor 4E-mediated recessive resistance to plant viruses and its utility in crop improvement. Mol Plant Pathol 13:795–803

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto Y (1992) Studies on breeding of tobacco varieties resistant to veinal necrosis disease by potato virus Y strain T. Bull Leaf Tob Res Lab 2:1–85

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Imperial Tobacco Bergerac, La Tour, F-24100, Bergerac, France

    E. Julio, J. Cotucheau, C. Decorps, R. Volpatti, C. Sentenac & F. Dorlhac de Borne

  2. UMR 1332 Biologie du Fruit et Pathologie, INRA et Université de Bordeaux, CS 20032, 33882, Villenave d’Ornon Cedex, France

    T. Candresse

Authors
  1. E. Julio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Cotucheau
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Decorps
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. Volpatti
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. Sentenac
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. T. Candresse
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. F. Dorlhac de Borne
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Julio.

Additional information

The sequence of contig S10760 is released in Genbank under the KF155696 accession number, as well as contig S15602 (KM202061), S04984 (KM202062), T013419 (KM202063), T014720 (KM202064), T024242 (KM202065), S10809 (KM202066), T015277 (KM202067), T021658 (KM202068), T021287 (KM202069), T025160 (KM202070), and S05588 (KM202071).

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM1

(DOC 40 kb).

ESM2

(DOC 32 kb).

ESM3

(DOC 101 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Julio, E., Cotucheau, J., Decorps, C. et al. A Eukaryotic Translation Initiation Factor 4E (eIF4E) is Responsible for the “va” Tobacco Recessive Resistance to Potyviruses. Plant Mol Biol Rep 33, 609–623 (2015). https://doi.org/10.1007/s11105-014-0775-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-014-0775-4

Keywords

Search

Navigation