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Although they are staple foods in cuisines globally, many commercial fruit varieties have become progressively less flavorful over time. Due to the cost and difficulty associated with flavor phenotyping, breeding programs have long been challenged in selecting for this complex trait. To address this issue, we leveraged targeted metabolomics of diverse tomato and blueberry accessions and their corresponding consumer panel ratings to create statistical and machine learning models that can predict sensory perceptions of fruit flavor. Using these models, a breeding program can assess flavor ratings for a large number of genotypes, previously limited by the low throughput of consumer sensory panels. The ability to predict consumer ratings of liking, sweet, sour, umami, and flavor intensity was evaluated by a 10-fold cross-validation, and the accuracies of 18 different models were assessed. The prediction accuracies were high for most attributes and ranged from 0.87 for sourness intensity in blueberry using XGBoost to 0.46 for overall liking in tomato using linear regression. Further, the best-performing models were used to infer the flavor compounds (sugars, acids, and volatiles) that contribute most to each flavor attribute. We found that the variance decomposition of overall liking score estimates that 42% and 56% of the variance was explained by volatile organic compounds in tomato and blueberry, respectively. We expect that these models will enable an earlier incorporation of flavor as breeding targets and encourage selection and release of more flavorful fruit varieties. 

Abstract Methyl salicylate imparts a potent flavor and aroma described as medicinal and wintergreen that is undesirable in tomato (Solanum lycopersicum) fruit. Plants control the quantities of methyl salicylate through a variety of biosynthetic pathways, including the methylation of salicylic acid to form methyl salicylate and subsequent glycosylation to prevent methyl salicylate emission. Here, we identified a subclade of tomato methyl esterases, SALICYLIC ACID METHYL ESTERASE1-4, responsible for demethylation of methyl salicylate to form salicylic acid in fruits. This family was identified by proximity to a highly significant methyl salicylate genome-wide association study locus on chromosome 2. Genetic mapping studies in a biparental population confirmed a major methyl salicylate locus on chromosome 2. Fruits from SlMES1 knockout lines emitted significantly (P < 0,05, t test) higher amounts of methyl salicylate than wild-type fruits. Double and triple mutants of SlMES2, SlMES3, and SlMES4 emitted even more methyl salicylate than SlMES1 single knockouts—but not at statistically distinguishable levels—compared to the single mutant. Heterologously expressed SlMES1 and SlMES3 acted on methyl salicylate in vitro, with SlMES1 having a higher affinity for methyl salicylate than SlMES3. The SlMES locus has undergone major rearrangement, as demonstrated by genome structure analysis in the parents of the biparental population. Analysis of accessions that produce high or low levels of methyl salicylate showed that SlMES1 and SlMES3 genes expressed the highest in the low methyl salicylate lines. None of the MES genes were appreciably expressed in the high methyl salicylate-producing lines. We concluded that the SlMES gene family encodes tomato methyl esterases that convert methyl salicylate to salicylic acid in ripe tomato fruit. Their ability to decrease methyl salicylate levels by conversion to salicylic acid is an attractive breeding target to lower the level of a negative contributor to flavor. 

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. 

SUMMARY The unique flavors of different fruits depend upon complex blends of soluble sugars, organic acids, and volatile organic compounds. 2‐Phenylethanol and phenylacetaldehyde are major contributors to flavor in many foods, including tomato. In the tomato fruit, glucose, and fructose are the chemicals that most positively contribute to human flavor preferences. We identified a gene encoding a tomato aldo/keto reductase,Sl‐AKR9, that is associated with phenylacetaldehyde and 2‐phenylethanol contents in fruits. Two distinct haplotypes were identified; one encodes a chloroplast‐targeted protein while the other encodes a transit peptide‐less protein that accumulates in the cytoplasm. Sl‐AKR9 effectively catalyzes reduction of phenylacetaldehyde to 2‐phenylethanol. The enzyme can also metabolize sugar‐derived reactive carbonyls, including glyceraldehyde and methylglyoxal. CRISPR‐Cas9‐induced loss‐of‐function mutations inSl‐AKR9significantly increased phenylacetaldehyde and lowered 2‐phenylethanol content in ripe fruit. Reduced fruit weight and increased soluble solids, glucose, and fructose contents were observed in the loss‐of‐function fruits. These results reveal a previously unidentified mechanism affecting two flavor‐associated phenylalanine‐derived volatile organic compounds, sugar content, and fruit weight. Modern varieties of tomato almost universally contain the haplotype associated with larger fruit, lower sugar content, and lower phenylacetaldehyde and 2‐phenylethanol, likely leading to flavor deterioration in modern varieties.