A flavin-dependent monooxygenase produces nitrogenous tomato aroma volatiles using cysteine as a nitrogen source
Tomato ( ) 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 nitrogenou...
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| Published in: | Proceedings of the National Academy of Sciences - PNAS Vol. 119; no. 7 |
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| Main Authors: | , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
National Academy of Sciences
15-02-2022
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| Subjects: | |
| Online Access: | Get full text |
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| Summary: | Tomato (
) 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
are nearly devoid, while the red-fruited species
and
accumulate high amounts. Using an introgression population derived from
, we identified a locus essential for the production of all the detectable nitrogenous volatiles in tomato fruit. Silencing of the underlying gene (
;
) 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.
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
-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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| Bibliography: | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Contributed by Harry J. Klee; received October 11, 2021; accepted December 17, 2021; reviewed by Mark Lange and Sarah O’Connor 2Present address: College of Bioresource Sciences and Graduate School of Bioresource Sciences, Nihon University, Fujisawa, Kanagawa, 252-0880, Japan. Author contributions: D.K.L., Y.K., H.J.K., and C.G. designed research; D.K.L., Y.K., J.G., C.J.K., K.H., B.B., N.B.L., L.F.N., D.M.T., and C.G. performed research; D.K.L., V.K., J.M., and M.P. contributed new reagents/analytic tools; D.K.L., Y.K., J.G., C.J.K., K.H., B.B., V.K., J.M., and C.G. analyzed data; and D.K.L., Y.K., H.J.K., and C.G. wrote the paper. 1D.K.L. and Y.K. contributed equally to this work. |
| ISSN: | 0027-8424 1091-6490 |
| DOI: | 10.1073/pnas.2118676119 |