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Theoretical and Applied Genetics

, Volume 120, Issue 1, pp 191–200 | Cite as

Non-synonymous single nucleotide polymorphisms in the watermelon eIF4E gene are closely associated with resistance to Zucchini yellow mosaic virus

  • Kai-Shu LingEmail author
  • Karen R. Harris
  • Jenelle D. F. Meyer
  • Amnon Levi
  • Nihat Guner
  • Todd C. Wehner
  • Abdelhafid Bendahmane
  • Michael J. Havey
Original Paper

Abstract

Zucchini yellow mosaic virus (ZYMV) is one of the most economically important potyviruses infecting cucurbit crops worldwide. Using a candidate gene approach, we cloned and sequenced eIF4E and eIF(iso)4E gene segments in watermelon. Analysis of the nucleotide sequences between the ZYMV-resistant watermelon plant introduction PI 595203 (Citrullus lanatus var. lanatus) and the ZYMV-susceptible watermelon cultivar ‘New Hampshire Midget’ (‘NHM’) showed the presence of single nucleotide polymorphisms (SNPs). Initial analysis of the identified SNPs in association studies indicated that SNPs in the eIF4E, but not eIF(iso)4E, were closely associated to the phenotype of ZYMV-resistance in 70 F2 and 114 BC1R progenies. Subsequently, we focused our efforts in obtaining the entire genomic sequence of watermelon eIF4E. Three SNPs were identified between PI 595203 and NHM. One of the SNPs (A241C) was in exon 1 and the other two SNPs (C309A and T554G) were in the first intron of the gene. SNP241 which resulted in an amino acid substitution (proline to threonine) was shown to be located in the critical cap recognition and binding area, similar to that of several plant species resistance to potyviruses. Analysis of a cleaved amplified polymorphism sequence (CAPS) marker derived from this SNP in F2 and BC1R populations demonstrated a cosegregation between the CAPS-2 marker and their ZYMV resistance or susceptibility phenotype. When we investigated whether such SNP mutation in the eIF4E was also conserved in several other PIs of C. lanatus var. citroides, we identified a different SNP (A171G) resulting in another amino acid substitution (D71G) from four ZYMV-resistant C. lanatus var. citroides (PI 244018, PI 482261, PI 482299, and PI 482322). Additional CAPS markers were also identified. Availability of all these CAPS markers will enable marker-aided breeding of watermelon for ZYMV resistance.

Keywords

Amplify Fragment Length Polymorphism Melon Plant Introduction Disease Severity Index Zucchini Yellow Mosaic Virus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Andrea Gilliard, Emily Walters, and Laura Pence for their excellent technical assistance, and Drs. W. Patrick Wechter and Ryan Donahoo for their critical readings to the manuscript.

References

  1. Albar L, Bangratz-Reyser M, Eugenie H, Marie-Noelle N, Jones M, Ghesquiere A (2006) Mutations in the eIF(iso)4G translation initiation factor confer high resistance of rice to Rice yellow mottle virus. Plant J 47:417–426CrossRefPubMedGoogle Scholar
  2. Boyhan G, Norton JD, Jacobsen BJ, Abrahams BR (1992) Evaluation of watermelon and related germplasm for resistance to Zucchini yellow mosaic virus. Plant Dis 76:251–252Google Scholar
  3. Boyhan GE, Krewer G, Granberry DM, Hill CR, Mills WA (2007) ‘Orange Bulldog’, a virus-resistant pumpkin for fall production in the Southeast. HortScience 42:1484–1485Google Scholar
  4. Charron C, Nicolai M, Gallois JL, Robaglia C, Moury B, Palloix A, Caranta C (2008) Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J 54:56–68CrossRefPubMedGoogle Scholar
  5. 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 32:927–934CrossRefPubMedGoogle Scholar
  6. FAO (2007) Agricultural statistics for 2007. Food and Agriculture Organization of the United Nations. http://faostat.fao.org/
  7. Gao Z, Johansen E, Eyers S, Thomas C, Ellis T, Maule A (2004) The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J 40:376–385CrossRefPubMedGoogle Scholar
  8. Guner N (2004) Papaya ringspot virus watermelon strain and Zucchini yellow mosaic virus resistance in watermelon. PhD Dissertation, North Carolina State University, Raleigh, North Carolina, USAGoogle Scholar
  9. Kang BC, Yeam I, Frantz JD, Murphy JF, Jahn MM (2005a) The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant J 42:392–405CrossRefPubMedGoogle Scholar
  10. Kang BC, Yeam I, Jahn MM (2005b) Genetics of plant virus resistance. Annu Rev Phytopathol 43:581–621CrossRefPubMedGoogle Scholar
  11. 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 5:526–536CrossRefGoogle Scholar
  12. 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 6:449–458CrossRefGoogle Scholar
  13. Lellis A, Kasschau K, Whitham S, Carrington J (2002) Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr Biol 12:1046–1051CrossRefPubMedGoogle Scholar
  14. Levi A, Thomas CE, Joobeur T, Zhang X, Davis A (2002) A genetic linkage map for watermelon derived from a testcross population: (Citrullus lanatus var. citroides × C. lanatus var. lanatus) × Citrullus colocynthis. Theor Appl Genet 105:555–563CrossRefPubMedGoogle Scholar
  15. Levi A, Thomas CE, Trebitsh T, Salman A, King J, Karalius J, Newman M, Reddy OUK, Xu Y, Zhang X (2006) An extended linkage map for watermelon based on SRAP, AFLP, SSR, ISSR, and RAPD markers. J Am Soc Hortic Sci 131:393–402Google Scholar
  16. Lisa V, Lecoq H (1984) Zucchini yellow mosaic virus. No. 282. CMI/AAB Descriptions of plant viruses. Ferry Lane, Kew, Surrey, England, p 4Google Scholar
  17. Ma SQ, Xu Y, Gong GY, Zhang HY, Shen HL (2005) Analysis on the inheritance to PRSV-W and ZYMV-CH and their linkage in watermelon. J Fruit Sci 22:731–733Google Scholar
  18. Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK (1997) Cocrystal structure of the messager RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell 89:951–961CrossRefPubMedGoogle Scholar
  19. Maule A, Caranta C, Boulton M (2007) Sources of natural resistance to plant viruses: status and prospects. Mol Plant Pathol 8:223–231CrossRefGoogle Scholar
  20. Meyer JDF, Deleu W, Garcia-Mas J, Havey MJ (2008) Construction of a fosmid library of cucumber (Cucumis sativus) and comparative analysis of the eIF4E and eIF(iso)4E regions from cucumber and melon (Cucumis melo). Mol Genet Genomics 279:473–480CrossRefPubMedGoogle Scholar
  21. Michon T, Estevez Y, Walter J, German-Retana S, Le Gall O (2006) The potyviral virus genome-linked protein VPg forms a ternary complex with the eukaryotic initiation factors eIF4E and eIF4G and reduces eIF4E affinity for a mRNA cap analogue. FEBS J 273:1312–1322CrossRefPubMedGoogle Scholar
  22. Monzingo AF, Dhaliwal S, Dutt-Chaudhuri A, Lyon A, Sadow JH, Hoffman DW, Robertus JD, Browning KS (2007) The structure of translation initiation factor eIF4E from wheat reveals a novel disulfide bond. Plant Physiol 143:1504–1518CrossRefPubMedGoogle Scholar
  23. Nicaise V, German-Retana S, Sanjuan R, Dubrana MP, Mazier M, Maisonneuve B, Candresse T, Caranta C, Le Gall O (2003) The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the potyvirus Lettuce mosaic virus. Plant Physiol 132:1272–1282CrossRefPubMedGoogle Scholar
  24. Nieto C, Morales M, Orjeda G, Clepet C, Monfort A, Sturbois B, Puigdomenech 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 48:452–462CrossRefPubMedGoogle Scholar
  25. Provvidenti R (1991) Inheritance of resistance to the Florida strain of Zucchini yellow mosaic virus in watermelon. HortScience 26:407–408Google Scholar
  26. Provvidenti R (1996) Zucchini yellow mosaic virus. In: Zitter TA, Hopkins DL, Thomas CE (eds) Compendium of cucurbit diseases. APS Press, St. Paul, Minnesota, p 44Google Scholar
  27. Provvidenti R, Hampton RO (1992) Sources of resistance to potyviruses. In: Potyvirus taxonomy. Arch Virol (Suppl. 5):189–211Google Scholar
  28. Provvidenti R, Gonsalves D, Humaydan HS (1984) Occurrence of Zucchini yellow mosaic virus in cucurbits from Connecticut, New York, Florida, and California. Plant Dis 68:443–446CrossRefGoogle Scholar
  29. Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11:40–45CrossRefPubMedGoogle Scholar
  30. 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 32:1067–1075CrossRefPubMedGoogle Scholar
  31. 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 274:346–353CrossRefPubMedGoogle Scholar
  32. 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 87:2089–2098CrossRefPubMedGoogle Scholar
  33. 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 579:1167–1171CrossRefPubMedGoogle Scholar
  34. 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 42:912–922CrossRefPubMedGoogle Scholar
  35. Van Ooijen JW, Voorrips RE (2001) JoinMap® 3.0, software for the calculation of genetic linkage maps. Plant Research International, Wageningen, the NetherlandsGoogle Scholar
  36. Xu Y, Kang D, Shi Z, Shen H, Wehner T (2004) Inheritance of resistance to Zucchini yellow mosaic virus and Watermelon mosaic virus in watermelon. J Hered 95:498–502CrossRefPubMedGoogle Scholar
  37. Yeam I, Kang B, Lindeman W, Frantz J, Faber N, Jahn M (2005) Allele-specific CAPS markers based on point mutations in resistance allele at the pvr1 locus encoding eIF4E in Capsicum. Theor Appl Genet 112:178–186CrossRefPubMedGoogle Scholar
  38. Yeam I, Cavatorta JR, Ripoll D, Kang BC, Jahn MM (2007) Functional dissection of naturally occurring amino acid substitutions in eIF4E that confers recessive potyvirus resistance in plants. Plant Cell 19:2913–2928CrossRefPubMedGoogle Scholar
  39. 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. Virology 78:6102–6111CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Kai-Shu Ling
    • 1
    Email author
  • Karen R. Harris
    • 1
  • Jenelle D. F. Meyer
    • 2
  • Amnon Levi
    • 1
  • Nihat Guner
    • 3
  • Todd C. Wehner
    • 3
  • Abdelhafid Bendahmane
    • 4
  • Michael J. Havey
    • 2
  1. 1.U.S. Vegetable LaboratoryU.S. Department of Agriculture, Agriculture Research ServiceCharlestonUSA
  2. 2.U.S. Department of Agriculture, Agriculture Research Service, Department of HorticultureUniversity of WisconsinMadisonUSA
  3. 3.Department of Horticultural ScienceNorth Carolina State UniversityRaleighUSA
  4. 4.INRA (Institut National de la Recherche Agronomique) – CNRS, UMR1165Unité de Recherche en Génomique VégétaleEvryFrance

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