European Journal of Plant Pathology

, Volume 121, Issue 2, pp 189–194 | Cite as

Functional degeneration of the resistance gene nsv against Melon necrotic spot virus at low temperature

  • Kazutaka Kido
  • Tomofumi Mochizuki
  • Kazutoshi Matsuo
  • Chika Tanaka
  • Kenji Kubota
  • Takehiro Ohki
  • Shinya Tsuda
Article
First Online:
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Accepted:

Abstract

The single recessive gene, nsv, which confers resistance against Melon necrotic spot virus (MNSV), has recently been used to develop virus-resistant melon cultivars in Japan. However, the Chiba isolate of MNSV, a common isolate in Japan, infected resistant cultivars when inoculated melon plants were grown at 15°C. Viral RNAs accumulated in protoplasts from resistant cultivars at both 15 and 20°C. Mechanical inoculation of the cotyledons caused MNSV to spread throughout the leaves at 15°C, but not at 20°C. These results support our novel hypothesis that a temperature-sensitive inactivation of disease resistance genes occurs at the nsv locus in melon cultivars with the resistance gene grown at temperatures below 20°C.

Keywords

Cell-to-cell movement Methyl bromide Olpidium bornovanus Protoplast Recessive resistance Viral replication 

Abbreviations

DAS-ELISA

double-antibody sandwich enzyme-linked immunosorbent assay

dpi

days post-inoculation

eIF4E

eukaryotic initiation factor 4E

hpi

hours post-inoculation

IgG

immunoglobulin G

MNSV

Melon necrotic spot virus

PBS

phosphate-buffered saline

USDA-ARS

United States Department of Agriculture Agricultural Research Station

UTR

untranslated region

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Notes

Acknowledgements

We are grateful to T. Meshi for helpful comments and discussion. We also thank L.M. Knight for critical reading of this manuscript. This study was supported, in part, by a Grant-in-Aid as part of The Research Project for Utilizing Advanced Technologies in Agriculture, Forestry and Fisheries administered by the Ministry of Agriculture, Forestry and Fisheries in Japan.

References

  1. Albar, L., Bangratz-Reyser, M., Hébrard, E., Ndjiondjop, M.-N., Jones, M., & Ghesquière, A. (2006). Mutations in the eIF(iso)4G translation initiation factor confer high resistance of rice to Rice yellow mottle virus. Plant Journal, 47, 417–426.PubMedCrossRefGoogle Scholar
  2. Avegelis, A. (1985). Occurrence of Melon necrotic spot virus in Crete (Greece). Phytopathologische Zeitschrift, 114, 365–372.CrossRefGoogle Scholar
  3. Campbell, R. N., & Sim, S. T. (1994). Host specificity and nomenclature of Olpidium bornovanus (= Olpidium radicale) and comparisons to Olpidium brassicae. Canadian Journal of Botany, 72, 1136–1143.CrossRefGoogle Scholar
  4. Campbell, R. N., Wipf-Scheibel, C., & Lecoq, H. (1996). Vector-assisted seed transmission of Melon necrotic spot virus in melon. Phytopathology, 86, 1294–1298.CrossRefGoogle Scholar
  5. Clark, M. F., & Adams, A. N. (1977). Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. Journal of General Virology, 34, 475–483.PubMedGoogle Scholar
  6. Coudriet, D. L., Kishaba, A. N., & Bohn, G. W. (1981). Inheritance of resistance to Muskmelon necrotic spot virus in a melon aphid-resistance breeding line of muskmelon. Journal of the American Society for Horticultural Science, 106, 789–791.Google Scholar
  7. Díaz, J. A., Nieto, C., Moriones, E., & Aranda, M. A. (2002). Spanish Melon necrotic spot virus isolate overcomes the resistance conferred by the recessive nsv gene of melon. Plant Disease, 86, 694.CrossRefGoogle Scholar
  8. Díaz, J. A., Nieto, C., Moriones, E., & Aranda, M. A. (2003). Nucleotide sequence and infectious transcripts from a full-length cDNA clone of the carmovirus Melon necrotic spot virus. Archives of Virology, 148, 599–607.PubMedCrossRefGoogle Scholar
  9. Díaz, J. A., Nieto, C., Moriones, E., Truniger, V., & Aranda, M. A. (2004). Molecular characterization of Melon necrotic spot virus strain that overcomes the resistance in melon and nonhost plans. Molecular Plant-Microbe Interactions, 17, 668–675.PubMedCrossRefGoogle Scholar
  10. Friedland, D. E., Wooten, W. N. B., LaVoy, J. E., Hagedorn, C. H., & Goss, D. J. (2005). A mutant of eukaryotic protein synthesis initiation factor eIF4k119A has an increased binding affinity for both m7G cap analogues and eIF4G peptides. Biochemistry, 44, 4546–4550.PubMedCrossRefGoogle Scholar
  11. Furuki, I. (1981). Epidemiological studies on Melon necrotic spot. Shizuoka (Japan) Agricultural Experiment Station Technical Bulletin No. 14. (Shizuoka Prefecture, Japan).Google Scholar
  12. Gao, Z., Johansen, E., Eyers, S., Thomas, C. L., Ellis, T. H. N., & 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 Journal, 40, 376–385.PubMedCrossRefGoogle Scholar
  13. Genovés, A., Navarro, J., & Pallás, V. (2006). Functional analysis of the five Melon necrotic spot virus genome-encoded proteins. Journal of General Virology, 87, 2371–2380.PubMedCrossRefGoogle Scholar
  14. Gonzalez-Garza, R., Gumpf, D. J., Kishaba, A. N., & Bohn, G. W. (1979). Identification, seed transmission, and host range pathogenicity of a California isolate of Melon necrotic spot virus. Phytopathology, 69, 340–345.CrossRefGoogle Scholar
  15. Hamilton, A. J., & Baulcombe, D. C. (1999). A species of small antisense RNA in post-transcriptional gene silencing in plants. Science, 286, 950–952.PubMedCrossRefGoogle Scholar
  16. Kanyuka, K., Druka, A., Caldwell, D. G., Tymon, A., Mccallum, N., Waugh, R., et al. (2005). Evidence that the recessive bymovirus resistance locus rym4 in barley corresponds to the eukaryotic translation initiation factor 4E gene. Molecular Plant Pathology, 6, 449–458.CrossRefPubMedGoogle Scholar
  17. Kido, K., Tanaka, C., Mochizuki, T., Kubota, K., Ohki, T., Ohnishi, J., et al. (2008). High temperatures activate local viral multiplication and cell-to-cell movement of Melon necrotic spot virus, but restrict expression of systemic symptoms. Phytopathology, in press.Google Scholar
  18. Kishi, K. (1966). Necrotic spot of melon, a new virus disease. Annals of the Phytopathological Society of Japan, 32, 138–144.Google Scholar
  19. Mochizuki, T., Ohnishi, J., Ohki, T., Kanda, A., & Tsuda, S. (2008). Amino-acid substitution in the coat protein of Melon necrotic spot virus causes loss of binding to the surface of Olpidium bornovanus zoospores. Journal of General Plant Pathology, in press.Google Scholar
  20. Navarro, J. A., Genovés, A., Climent, J., Saurí, A., Martínez-Gil, L., Mingarro, I., et al. (2006). RNA-binding properties and membrane insertion of Melon necrotic spot virus (MNSV) double gene block movement proteins. Virology, 356, 57–67.PubMedCrossRefGoogle Scholar
  21. Nieto, C., Moral, M., Orjeda, G., Clepet, C., Monfort, A., Sturbois, B., et al. (2006). An eIF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon. Plant Journal, 48, 1–11.CrossRefGoogle Scholar
  22. Nieto, C., Piron, F., Dalmais, M., Marco, C. F., Moriones, E., Gómez-Guillamón, M. L., et al. (2007). EcoTILLING for the identification of allelic variants of melon eIF4E, a factor that controls virus susceptibility. BMC Plant Biology, 21, 7–34.Google Scholar
  23. Robaglia, C., & Caranta, C. (2006). Translation initiation factors: a weak link in plant virus infection. Trends in Plant Science, 11, 40–45.PubMedCrossRefGoogle Scholar
  24. Ryden, K., & Person, P. (1986). Melon necrotic spot – A new virus disease in Sweden. Vaxtskyddsnotiser, 50, 130–132.Google Scholar
  25. Sato, M., Masuta, C., & Uyeda, I. (2003). Natural resistance to Clover yellow vein virus in beans controlled by a single recessive locus. Molecular Plant-Microbe Interactions, 16, 994–1002.PubMedCrossRefGoogle Scholar
  26. Stein, N., Perovic, D., Kumlehn, J., Pellio, B., Stracke, S., Streng, S., et al. (2005). The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). Plant Journal, 42, 912–922.PubMedCrossRefGoogle Scholar
  27. Yoshii, M., Nishikiori, M., Tomita, K., Yoshioka, N., Kozuka, R., Naito, S., et al. (2004). The Arabidopsis cucumovirus multiplication 1 and 2 loci encode translation initiation factors 4E and 4G. Journal of Virology, 78, 6102–6111.PubMedCrossRefGoogle Scholar
  28. Yoshii, M., Yoshioka, N., Ishikawa, M., & Naito, S. (1998). Isolation of an Arabidopsis thaliana mutant in which the multiplication of both Cucumber mosaic virus and Turnip crinkle virus is affected. Journal of Virology, 72, 8731–8737.PubMedGoogle Scholar
  29. Yosida, K., Goto, T., Nemoto, M., & Tsuchizaki, T. (1980). Five viruses isolated from melon in Hokkaido. Annals of the Phytopathological Society of Japan, 46, 339–348.Google Scholar

Copyright information

© KNPV 2007

Authors and Affiliations

  • Kazutaka Kido
    • 1
  • Tomofumi Mochizuki
    • 2
  • Kazutoshi Matsuo
    • 3
  • Chika Tanaka
    • 4
  • Kenji Kubota
    • 5
  • Takehiro Ohki
    • 2
  • Shinya Tsuda
    • 2
  1. 1.Yokohamaueki Co. LtdYokohamaJapan
  2. 2.National Agricultural Research CentreTsukubaJapan
  3. 3.Nagasaki Agricultural and Forestry Experiment StationIsahayaJapan
  4. 4.Southern Prefectural Horticulture InstituteChiba Prefecture Agriculture Research CentreTateyamaJapan
  5. 5.National Agricultural Research Centre for Kyushu Okinawa RegionKikuchiJapan

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