An eIF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon

Cristina Nieto, Monica Morales, Gisella Orjeda, Christian Clepet, Amparo Monfort, Benedicte Sturbois, Pere Puigdomènech, Michel Pitrat, Michel Caboche, Catherine Dogimont, Jordi Garcia-Mas, Miguel A. Aranda, Abdelhafid Bendahmane

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136 Scopus citations

Abstract

The characterization of natural recessive resistance genes and virus-resistant mutants of Arabidopsis have implicated translation initiation factors of the 4E family [eIF4E and eIF(iso)4E] as susceptibility factors required for virus multiplication and resistance expression. To date, viruses controlled by these genes mainly belong to the family Potyviridae. Melon necrotic spot virus (MNSV) belongs to the family Tombusviridae (genus Carmovirus) and is an uncapped and non-polyadenylated RNA virus. In melon, nsv-mediated resistance is a natural source of recessive resistance against all strains of MNSV except MNSV-264. Analyses of chimeras between non-resistance-breaking and resistance-breaking strains have shown that the avirulence determinant maps to the 3′-untranslated region (3′-UTR) of the viral genome. Using a combination of positional cloning and microsynteny analysis between Arabidopsis thaliana and melon, we genetically and physically delimited the nsv locus to a single bacterial artificial chromosome clone and identified the melon eukaryotic translation initiation factor 4E (Cm-eIF4E) as a candidate gene. Complementation analysis using a biolistic transient expression assay, confirmed Cm-eIF4E as the product of nsv. A single amino acid change at position 228 of the protein led to the resistance to MNSV. Protein expression and cap-binding analysis showed that Cm-eIF4E encoded by a resistant plant was not affected in it's cap-binding activity. The Agrobacterium-mediated transient expression of the susceptibility allele of Cm-eIF4E in Nicotiana benthamiana enhanced MNSV-264 accumulation. Based on these results, a model to explain melon resistance to MNSV is proposed. These data, and data from other authors, suggest that translation initiation factors of the eIF4E family are universal determinants of plant susceptibility to RNA viruses. © 2006 INRA.
Original languageAmerican English
Pages (from-to)452-462
Number of pages11
JournalPlant Journal
DOIs
StatePublished - 1 Jan 2006
Externally publishedYes

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    Nieto, C., Morales, M., Orjeda, G., Clepet, C., Monfort, A., Sturbois, B., Puigdomènech, P., Pitrat, M., Caboche, M., Dogimont, C., Garcia-Mas, J., Aranda, M. A., & Bendahmane, A. (2006). An eIF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon. Plant Journal, 452-462. https://doi.org/10.1111/j.1365-313X.2006.02885.x