Flavor and quality are the major drivers of fruit consumption in the US. However, the poor flavor of modern commercial tomato varieties is a major cause of consumer dissatisfaction. Studies in flavor research have informed the role of volatile organic compounds in improving overall liking and sweetness of tomatoes. These studies have utilized and applied the tools of molecular biology, genetics, biochemistry, omics, machine learning, and gene editing to elucidate the compounds and biochemical pathways essential for good tasting fruit. Here, we discuss the progress in identifying the biosynthetic pathways and chemical modifications of important tomato volatile compounds. We also summarize the advances in developing highly flavorful tomato varieties and future steps toward developing a “perfect tomato”.
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Metabolomic selection for enhanced fruit flavor
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.
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- Award ID(s):
- 1855585
- NSF-PAR ID:
- 10321895
- 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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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‐AKR9 significantly 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. -
null (Ed.)Fruit flavor is defined as the perception of the food by the olfactory and gustatory systems, and is one of the main determinants of fruit quality. Tomato flavor is largely determined by the balance of sugars, acids and volatile compounds. Several genes controlling the levels of these metabolites in tomato fruit have been cloned, including LIN5 , ALMT9 , AAT1 , CXE1 , and LoxC . The aim of this study was to identify any association of these genes with trait variation and to describe the genetic diversity at these loci in the red-fruited tomato clade comprised of the wild ancestor Solanum pimpinellifolium , the semi-domesticated species Solanum lycopersicum cerasiforme and early domesticated Solanum lycopersicum . High genetic diversity was observed at these five loci, including novel haplotypes that could be incorporated into breeding programs to improve fruit quality of modern tomatoes. Using newly available high-quality genome assemblies, we assayed each gene for potential functional causative polymorphisms and resolved a duplication at the LoxC locus found in several wild and semi-domesticated accessions which caused lower accumulation of lipid derived volatiles. In addition, we explored gene expression of the five genes in nine phylogenetically diverse tomato accessions. In general, the expression patterns of these genes increased during fruit ripening but diverged between accessions without clear relationship between expression and metabolite levels.more » « less
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Societal Impact Statement Fleshy fruits provide humans with many flavorful and nutritious crops. Understanding the diversity of these plants is fundamental to managing agriculture and food security in a changing world. This study surveyed fruit trait variation across species of tomato wild relatives and explored associations among color, size, shape, sugars, and acids. These wild tomato species native to South America can be interbred with the economically important cultivated tomato. Beyond its application to tomatoes, deepening our knowledge of how fruit traits evolve together is valuable to crop improvement efforts aimed at breeding more nutritious and appealing varieties of fruits.
Summary Fleshy fruits display a striking diversity of traits, many of which are important for agriculture. The evolutionary drivers of this variation are not well understood, and most studies have relied on variation found in the wild. Few studies have explored this question on a fine‐grained scale with a group of recently diverged species while controlling for environmental effects.
We developed the tomato clade as a novel system for fruit trait evolution research by presenting the first common garden‐based systematic survey of variation and phylogenetic signal in color, nutrition, and morphology traits across all 13 species of tomato wild relatives (
Solanum s ect.Lycopersicon ). We laid the groundwork for further testing of potential evolutionary drivers by assessing patterns of clustering and correlation among disperser‐relevant fruit traits as well as historical climate variables.We found evidence of two distinct clusters of associated fruit traits defined by color, sugar type, and malic acid concentration. We also observed correlations between a fruit's external appearance and internal nutrient content that could function as honest signals to dispersers. Analyses of historical climate and soil variables revealed an association between red/orange/yellow fruits and high annual average temperature.
Our results establish the tomato clade as a promising system for testing hypotheses on the drivers of divergence behind early‐stage fleshy fruit evolution, particularly selective pressure from frugivores.
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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.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.2115865119
