A plant resistance mechanism that promotes the emergence of resistance-breaking variants of potato Y potyvirus

Abstract

Tobacco Virgin A Mutant (VAM) exhibits apparent immunity to several potyviruses in a strain-specific manner. Its resistance was generated by UV irradiation, and is partially conditioned by the recessive gene va. This allele has been introgressed into several breeding fines such as NC745. Previously, it was observed that the inoculation of an avirulent strain of potato Y potyvirus (PVY(NN)) in both resistant genotypes, caused systemic infection in some NC745 plants only, and the virus recovered from these plants acquired an ability to easily infect both NC745 and VAM. The current study was to identify the host factors that define each one of these resistant phenotypes, and to characterize the pathogenic properties of the evolving virus. VAM cells supported a reduced rate of PVY(NN)-accumulation compared with NC745 cells, which accumulated virus progeny at, he same level as the susceptible control Burley 21 (B21). However, in both resistant tobaccos the virus cell-to-cell movement was similarly impaired. Even so, PVY(NN) was recovered sooner from NC745- than from VAM-inoculated leaves. After PVY(NN)-detection, emerging resistance breaking (RB) variants were also recovered. Surprisingly, just in VAM, the RB variants never moved out of the inoculated leaves, until they were reinoculated in the same or another uninoculated VAM plant. The inability of the emerging RB variants to exit the PVY(NN)-inoculated VAM leaves was associated with their low accumulation rate and an obstruction imposed by coinfecting avirulent genotypes. The VAM factor restricting virus accumulation was inherited independently from va and operated in an allele doses manner. This gene, named rvam2, was easily overcome by the isolated RB variants, but the underlying virus modification(s) implied a loss of fitness in B21. Thus, the systemic emergence of RB variants, starting from a quasispecies, adapted to accumulate in Rvam2 genotypes (e.g., B21), seems to require a high rate of local virus accumulation linked to a selective constraint in the virus intercellular and/or intertissular traffic. This is the first report where the combined action of two vulnerable resistance mechanisms confers a stronger plant resistance to a viral systemic infection.