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Abstract PremiseThe 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 biosynthetic 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 (Solanumsect.Lycopersicon), with implications for crop improvement since these compounds are key components of tomato flavor. MethodsWe analyzed ripe fruit volatiles from 13 species of wild tomato grown in a common garden. Interspecific variations in 66 compounds and their biosynthetic pathways were assessed in 32 accessions, and an accession‐level phylogeny was constructed to account for relatedness. ResultsWild tomato species can be differentiated by their VOCs, withSolanum pennelliinotably distinct. Phylogenetic conservatism exists to a limited extent. Major cladewide patterns corresponded to divergence of the five brightly 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. ConclusionsWe 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 biosynthetic pathways for esters and nitrogen‐containing compounds, volatiles important to tomato flavor.
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A flavin-dependent monooxygenase produces nitrogenous tomato aroma volatiles using cysteine as a nitrogen source
Tomato ( Solanum lycopersicum ) produces a wide range of volatile chemicals during fruit ripening, generating a distinct aroma and contributing to the overall flavor. Among these volatiles are several aromatic and aliphatic nitrogen-containing compounds for which the biosynthetic pathways are not known. While nitrogenous volatiles are abundant in tomato fruit, their content in fruits of the closely related species of the tomato clade is highly variable. For example, the green-fruited species Solanum pennellii are nearly devoid, while the red-fruited species S. lycopersicum and Solanum pimpinellifolium accumulate high amounts. Using an introgression population derived from S. pennellii , we identified a locus essential for the production of all the detectable nitrogenous volatiles in tomato fruit. Silencing of the underlying gene ( SlTNH1 ; Solyc12g013690 ) in transgenic plants abolished production of aliphatic and aromatic nitrogenous volatiles in ripe fruit, and metabolomic analysis of these fruit revealed the accumulation of 2-isobutyl-tetrahydrothiazolidine-4-carboxylic acid, a known conjugate of cysteine and 3-methylbutanal. Biosynthetic incorporation of stable isotope-labeled precursors into 2-isobutylthiazole and 2-phenylacetonitrile confirmed that cysteine provides the nitrogen atom for all nitrogenous volatiles in tomato fruit. Nicotiana benthamiana plants expressing SlTNH1 readily transformed synthetic 2-substituted tetrahydrothiazolidine-4-carboxylic acid substrates into a mixture of the corresponding 2-substituted oxime, nitro, and nitrile volatiles. Distinct from other known flavin-dependent monooxygenase enzymes in plants, this tetrahydrothiazolidine-4-carboxylic acid N -hydroxylase catalyzes sequential hydroxylations. Elucidation of this pathway is a major step forward in understanding and ultimately improving tomato flavor quality.
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- Award ID(s):
- 1855585
- PAR ID:
- 10410292
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 119
- Issue:
- 7
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.2118676119
