NON-SMOKY GLYCOSYLTRANSFERASE1 Prevents the Release of Smoky Aroma from Tomato Fruit[W][OPEN]

The activity of NON-SMOKY GLYCOSYLTRANSFERASE1 (NSGT1) mediates the conversion of hydrolysis-susceptible glycosides of phenylpropanoid volatiles into hydrolysis-resistant forms and prevents damage-induced release of these volatiles in tomato fruit. This leads to a perceivable reduction in the smoky aroma intensity of these fruits compared to fruits of cultivars containing a truncated NSGT1 gene. Phenylpropanoid volatiles are responsible for the key tomato fruit (Solanum lycopersicum) aroma attribute termed “smoky.” Release of these volatiles from their glycosylated precursors, rather than their biosynthesis, is the major determinant of smoky aroma in cultivated tomato. Using a combinatorial omics approach, we identified the NON-SMOKY GLYCOSYLTRANSFERASE1 (NSGT1) gene. Expression of NSGT1 is induced during fruit ripening, and the encoded enzyme converts the cleavable diglycosides of the smoky-related phenylpropanoid volatiles into noncleavable triglycosides, thereby preventing their deglycosylation and release from tomato fruit upon tissue disruption. In an nsgt1/nsgt1 background, further glycosylation of phenylpropanoid volatile diglycosides does not occur, thereby enabling their cleavage and the release of corresponding volatiles. Using reverse genetics approaches, the NSGT1-mediated glycosylation was shown to be the molecular mechanism underlying the major quantitative trait locus for smoky aroma. Sensory trials with transgenic fruits, in which the inactive nsgt1 was complemented with the functional NSGT1, showed a significant and perceivable reduction in smoky aroma. NSGT1 may be used in a precision breeding strategy toward development of tomato fruits with distinct flavor phenotypes.