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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‐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.
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A tomato LATERAL ORGAN BOUNDARIES transcription factor, SlLOB1 , predominantly regulates cell wall and softening components of ripening
Fruit softening is a key component of the irreversible ripening program, contributing to the palatability necessary for frugivore-mediated seed dispersal. The underlying textural changes are complex and result from cell wall remodeling and changes in both cell adhesion and turgor. While a number of transcription factors (TFs) that regulate ripening have been identified, these affect most canonical ripening-related physiological processes. Here, we show that a tomato fruit ripening–specific LATERAL ORGAN BOUNDRIES ( LOB ) TF, SlLOB1 , up-regulates a suite of cell wall–associated genes during late maturation and ripening of locule and pericarp tissues. SlLOB1 repression in transgenic fruit impedes softening, while overexpression throughout the plant under the direction of the 35s promoter confers precocious induction of cell wall gene expression and premature softening. Transcript and protein levels of the wall-loosening protein EXPANSIN1 ( EXP1 ) are strongly suppressed in Sl LOB1 RNA interference lines, while EXP1 is induced in Sl LOB1 -overexpressing transgenic leaves and fruit. In contrast to the role of ethylene and previously characterized ripening TFs, which are comprehensive facilitators of ripening phenomena including softening, Sl LOB1 participates in a regulatory subcircuit predominant to cell wall dynamics and softening.
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- Award ID(s):
- 1855585
- PAR ID:
- 10321981
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 118
- Issue:
- 33
- 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.2102486118
