cmv1 encodes a vacuolar protein sorting 41 involved in vesicle trafficking to the vacuole and determines cucumber mosaic virus transport to the phloem

Abstract

Infections by Cucumber mosaic virus (CMV), the type member of the Cucumovirus genus, can cause complete harvest loss in more than 1000 plant species, including important crop plants. CMV is classified in two subgroups (I and II) differing in 70% nucleotide sequence. The search for naturally resistant cultivars is a successful control measurement against viral infections. In the melon accession PI 161375, cultivar 'Songwhan Charmi' (SC), the resistance to CMV is mediated by a complex mixture of qualitative and quantitative genes. One single gene, cmv1, confers by itself total recessive resistance to strains of subgroup II by preventing viral transport from the bundle sheath cells, which surround the vein, to the phloem. To confer resistance to the subgroup I strains, at least two other QTLs must act together and cooperatively with cmv1. Here, we report the fine mapping and cloning of cmv1, encoding a Vacuolar Protein Sorting 41 (CmVPS41), a gene conserved among plants, animals and yeast, which is required for post Golgi vesicle trafficking towards the vacuole. We have screened a recombinant population of more than 4000 F2 plants and narrowed the region carrying cmv1 to 132 Kb including the CmVPS41 gene. We have validated CmVPS41 as cmv1 by generating susceptible SC transgenic lines, expressing the CmVPS41 allele from a susceptible genotype and by analyzing TILLING mutants with increased resistance to CMV. Besides, we analyzed a collection of genotypes and identified, by association, the mutation responsible for the resistance to CMV. CmVPS41 cellular function suggests that CMV might use part of CmVPS41 activity in the bundle sheath cell for its own transport towards the phloem cells to develop a systemic infection.