Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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Double Mutations in eIF4E and eIFiso4E Confer Recessive Resistance to Chilli Veinal Mottle Virus in Pepper

  • Hwang, JeeNa (Department of Plant Science, Plant Genomics and Breeding Institute, and Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Li, Jinjie (Department of Plant Science, Plant Genomics and Breeding Institute, and Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Liu, Wing-Yee (Department of Plant Science, Plant Genomics and Breeding Institute, and Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • An, Song-Ji (Department of Plant Science, Plant Genomics and Breeding Institute, and Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Cho, Hwajin (Molecular Markers Diagnostics Laboratory, Plant Breeding and NongWoo Bio Ltd.) ;
  • Her, Nam Han (Plant Pathology Laboratory, NongWoo Bio Ltd.) ;
  • Yeam, Inhwa (Plant Breeding and Genetics, Cornell University) ;
  • Kim, Dosun (National Institute of Horticultural and Herbal Science) ;
  • Kang, Byoung-Cheorl (Department of Plant Science, Plant Genomics and Breeding Institute, and Research Institute of Agriculture and Life Sciences, Seoul National University)
  • Received : 2008.10.09
  • Accepted : 2008.12.17
  • Published : 2009.03.31
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Abstract

To evaluate the involvement of translation initiation factors eIF4E and eIFiso4E in Chilli veinal mottle virus (ChiVMV) infection in pepper, we conducted a genetic analysis using a segregating population derived from a cross between Capsicum annuum 'Dempsey' containing an elF4E mutation ($pvr1^2$) and C. annuum 'Perennial' containing an elFiso4E mutation (pvr6). C. annuum 'Dempsey' was susceptible and C. annuum 'Perennial' was resistant to ChiVMV. All $F_1$ plants showed resistance, and $F_2$ individuals segregated in a resistant-susceptible ratio of 166:21, indicating that many resistance loci were involved. Seventy-five $F_2$ and 329 $F_3$ plants of 17 families were genotyped with $pvr1^2$ and pvr6 allele-specific markers, and the genotype data were compared with observed resistance to viral infection. All plants containing homozygous genotypes of both $pvr1^2$ and pvr6 were resistant to ChiVMV, demonstrating that simultaneous mutations in elF4E and eIFiso4E confer resistance to ChiVMV in pepper. Genotype analysis of $F_2$ plants revealed that all plants containing homozygous genotypes of both $pvr1^2$ and pvr6 showed resistance to ChiVMV. In protein-protein interaction experiments, ChiVMV viral genome-linked protein (VPg) interacted with both eIF4E and eIFiso4E. Silencing of elF4E and eIFiso4E in the VIGS experiment showed reduction in ChiVMV accumulation. These results demonstrated that ChiVMV can use both eIF4E and eIFiso4E for replication, making simultaneous mutations in eIF4E and eIFiso4E necessary to prevent ChiVMV infection in pepper.

Keywords

Acknowledgement

Supported by : Rural Development Administration, Ministry of Science and Technology

References

  1. Ahlquist, P., Noueiry, A.O., Lee, W.M., Kushner, D.B., and Dye, B.T. (2003). Host factors in positive-strand RNA virus genome replication. J. Virol. 77, 8181-8186 https://doi.org/10.1128/JVI.77.15.8181-8186.2003
  2. Caranta, C., Lefebvre, V., and Palloix, A. (1997). Polygenic resistance of pepper to potyviruses consists of a combination of isolate-specific and broad-spectrum quantitative trait loci. Mol. Plant Microbe Interact. 10, 872-878 https://doi.org/10.1094/MPMI.1997.10.7.872
  3. Charron, C., Nicolai, M., Gallois, J.-L., Robaglia, C., Moury, B., Palloix, A., and Caranta, C. (2008). Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J. 54, 56-68 https://doi.org/10.1111/j.1365-313X.2008.03407.x
  4. Chisholm, S.T., Coaker, G., Day, B., and Staskawicz, B.J. (2006). Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803-814 https://doi.org/10.1016/j.cell.2006.02.008
  5. Dangl, J.L. and Jones, J.D. (2001). Plant pathogens and integrated defence responses to infection. Nature 411, 826-833 https://doi.org/10.1038/35081161
  6. Gao, Z., Johansen, E., Eyers, S., Thomas, C.L., Noel Ellis, T.H., and Maule, A.J. (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 https://doi.org/10.1111/j.1365-313X.2004.02215.x
  7. Green, S.K., Hiskias, Y., Lesemann, D.E., and Vetten, H.J. (1999). Characterization of Chilli veinal mottle virus as a potyvirus distinct from Pepper veinal mottle virus. Petria 9, 332
  8. Grube, R.C., Radwanski, E.R., and Jahn, M. (2000a). Comparative genetics of disease resistance within the solanaceae. Genetics 155, 873-887
  9. Grube, R.C., Blauth, J.R., Arnedo-A, M.S., Caranta, C., and Jahn, M. (2000b). Identification and comparative mapping of a dominant potyvirus resistance gene cluster in Capsicum. Theor. Appl. Genet. 101, 852-859 https://doi.org/10.1007/s001220051552
  10. Grzela, R., Strokovska, L., Andrieu, J.P., Dublet, B., Zagorski, W.,and Chroboczek, J. (2006). Potyvirus terminal protein VPg, effector of host eukaryotic initiation factor eIF4E. Biochimie 88, 887-896 https://doi.org/10.1016/j.biochi.2006.02.012
  11. Kang, B.C., Yeam, I., and Jahn, M.M. (2005a). Genetics of plant virus resistance. Annu. Rev. Phytopathol. 43, 581-621 https://doi.org/10.1146/annurev.phyto.43.011205.141140
  12. Kang, B.C., Yeam, I., Frantz, J.D., Murphy, J.F., and Jahn, M.M. (2005b). The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant J. 42, 392-405 https://doi.org/10.1111/j.1365-313X.2005.02381.x
  13. Kang, B.C., Yeam, I., Li, H., Perez, K.W., and Jahn, M.M. (2007). Ectopic expression of a recessive resistance gene generates dominant potyvirus resistance in plants. Plant Biotechnol. J. 5, 526-536 https://doi.org/10.1111/j.1467-7652.2007.00262.x
  14. Kushner, D.B., Lindenbach, B.D., Grdzelishvili, V.Z., Noueiry, A.O., Paul, S.M., and Ahlquist, P. (2003). Systematic, genome-wide identification of host genes affecting replication of a positivestrand RNA virus. Proc. Natl. Acad. Sci. USA 100, 15764-15769 https://doi.org/10.1073/pnas.2536857100
  15. Kyle, M.M., and Palloix, A. (1997). Proposed revision of nomenclature for potyvirus resistance genes in Capsicum. Euphytica 97, 183-188 https://doi.org/10.1023/A:1003009721989
  16. Liu, Y., Schiff, M., and Dinesh-Kumar, S.P. (2002). Virus-induced gene silencing in tomato. Plant J. 31, 777-786 https://doi.org/10.1046/j.1365-313X.2002.01394.x
  17. Michelmore, R.W., and Meyers, B.C. (1998). Clusters of resistance genes in plants evolve by divergent selection and a birth-anddeath process. Genome Res. 8, 1113-1130 https://doi.org/10.1101/gr.8.11.1113
  18. Moury, B., Palloix, A., Caranta, C., Gognalons, P., Souche, S., Gebre Selassie, K., and Marchoux, G. (2005). Serological, molecular and pathotype diversity of Pepper veinal mottle virus and Chilli veinal mottle virus. Phytopathology 95, 227-232 https://doi.org/10.1094/PHYTO-95-0227
  19. Murphy, J.F., Blauth, J.R., Livingstone, K.D., Lackney, V.K., and Jahn, M. (1998). Genetic mapping of the pvr1 locus in Capsicum spp. and evidence that distinct potyvirus resistance loci control responses that differ at the whole plant and cellular levels. Mol. Plant Microbe Interact. 11, 943-951 https://doi.org/10.1094/MPMI.1998.11.10.943
  20. Nieto, C., Piron, F., Dalmais, M., Marco, C.F., Moriones, E., Gomez-Guillamon, M.L., Truniger, V., Gomez, P., Garcia-Mas, J., Aranda, M.A., et al. (2007). EcoTILLING for the identification of allelic variants of melon eIF4E, a factor that controls virus susceptibility. BMC Plant Biol. 7, 34 https://doi.org/10.1186/1471-2229-7-34
  21. Prince, J.P., Zhang, Y., Radwanski, E.R., and Kyle, M.M. (1997). A versatile and high-yielding protocol for the preparation of genomic DNA from Capsicum spp. (pepper). Hort. Sci. 32, 937-939
  22. Robaglia, C., and Caranta, C. (2006). Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci. 11, 40-45 https://doi.org/10.1016/j.tplants.2005.11.004
  23. Ruffel, S., Gallois, J.L., Moury, B., Robaglia, C., Palloix, A., and 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 https://doi.org/10.1099/vir.0.81817-0
  24. Sato, M., Nakahara, K., Yoshii, M., Ishikawa, M., and Uyeda, I. (2005). Selective involvement of members of the eukaryotic initiation factor 4E family in the infection of Aravidopsis thaliana by potyviruses. FEBS Lett. 579, 1167-1171 https://doi.org/10.1016/j.febslet.2004.12.086
  25. Siriwong, P., Kittipakorn, K., and Ikegami, M. (1995). Characterization of `Chilli veis-banding mottle virus isolated from pepper in Thailand. Plant Path. 44, 718-727 https://doi.org/10.1111/j.1365-3059.1995.tb01696.x
  26. Stein, N., Perovic, D., Kumlehn, J., Pellio, B., Stracke, S., Streng, S., Ordon, F., and Graner, A. (2005). The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). Plant J. 42, 912-922 https://doi.org/10.1111/j.1365-313X.2005.02424.x
  27. Tsai, W.S., Huang, Y.C., Zhang, D.Y., Reddy, K., Hidayat, S.H., Srithongchai, W., Green, S.K., and Jan, F.-J. (2008). Molecular characterization of the CP gene and 3′UTR of Chilli veinal mottle virus from South and Southeast Asia. Plant Path. 57, 408-416 https://doi.org/10.1111/j.1365-3059.2007.01780.x
  28. Wang, J., Liu, Z., Niu, S., Peng, M., and Wang, D. (2006). Natural occurrence of Chilli veinal mottle virus on Capsicum chinense in China. Plant Disease 90, 377 https://doi.org/10.1094/PD-90-0377C
  29. Yeam, I., Kang, B.C., Lindeman, W., Frantz, J.D., Faber, N., and Jahn, M.M. (2005). Allele-specific CAPS markers based on point mutations in resistance alleles at the pvr1 locus encoding eIF4E in Capsicum. Theor. Appl. Genet. 112, 178-186 https://doi.org/10.1007/s00122-005-0120-2
  30. Yeam, I., Cavatorta, J.R., Ripoll, D.R., Kang, B.C., and Jahn, M.M. (2007). Functional dissection of naturally occurring amino acid substitutions in eIF4E that confers recessive potyvirus resistance in plants. Plant Cell 19, 2913-2928 https://doi.org/10.1105/tpc.107.050997

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