Variation in ripe fruit volatiles across the tomato clade: an evolutionary framework for studying fruit scent diversity in a crop wild relative.

Abstract

The scents of volatile organic compounds (VOCs) are an important component of ripe fleshy fruit attractiveness, yet their variation across closely related wild species is poorly understood. Phylogenetic patterns in these compounds and their biochemical pathways offer insight into the evolutionary drivers of fruit diversity, including whether scent can communicate an honest signal of nutrient content to animal dispersers. We assessed ripe fruit VOC content across the tomato clade (Solanum sect. Lycopersicon), with implications for crop improvement since these compounds are key components of tomato flavor. We analyzed ripe fruit volatiles from 13 species of wild tomato grown under common garden conditions. Interspecific variation in 66 compounds and their biochemical pathways was assessed in 32 accessions, with an accession-level phylogeny accounting for relatedness. Wild tomato species can be differentiated by their VOCs, with Solanum pennellii notably distinct. Phylogenetic conservatism exists to a limited extent. Major clade-wide patterns corresponded to divergence of the five colored-fruited species from the nine green-fruited species, particularly for nitrogen-containing compounds (higher in colored-fruited) and esters (higher in green-fruited), the latter appearing to signal a sugar reward. We established a framework for fruit scent evolution studies in a crop wild relative system, showing that each species in the tomato clade has a unique VOC profile. Differences between color groups align with fruit syndromes that could be driven by selection from frugivores. The evolution of colored fruits was accompanied by changes in biochemical pathways underlying esters and nitrogen-containing compounds, volatiles important to tomato flavor. This article is protected by copyright. All rights reserved.