A phloem-based defense mechanism linked to elevated riboflavin levels in wild tomato Solanum chmielewskii impedes whitefly nymphal development

Abstract

Management of the phloem-feeding pest insect Bemisia tabaci (whitefly) is difficult due to its short generation time and large number of offspring. Several whitefly-resistant wild tomato accessions have been identified, with the resistance attributed to specific defense metabolites in glandular trichomes. Interestingly, we found that on Solanum chmielewskii LA1840, which lacks trichome-based resistance, nymphal development is delayed and decreased compared with a cultivated tomato. Here, we show that the resistance observed in LA1840 is based on a mobile factor in the vasculature, the site of interaction for nymphs during feeding. The putative compound responsible for the resistance apparently passed the graft junction from an LA1840 rootstock to an otherwise susceptible cultivar scion. After untargeted metabolomics on the phloem collected from the wild accessions, a Random Forest algorithm predicted riboflavin to be linked to the resistance phenotype. The resistant genotypes indeed exhibit increased riboflavin levels in leaves compared with susceptible plants. The effect of elevated riboflavin levels on whitefly nymph development was validated through feeding riboflavin to susceptible plants. Our results highlight the power of natural variation in metabolites and vasculature-based resistance mechanisms for the development of sustainable whitefly management.