Tomato aromatic amino acid decarboxylases participate in synthesis of the flavor volatiles 2-phenylethanol and 2-phenylacetaldehyde

Abstract

An important phenylalanine-derived volatile compound produced by plants is 2-phenylethanol. It is a major contributor to flavor in many foods, including fresh fruits, such as tomato, and an insectattracting scent in roses and many other flowers. Despite the centrality of 2-phenylethanol to flavor and fragrance, the plant genes responsible for its synthesis have not been identified. Here, we describe a biosynthetic pathway for 2-phenylethanol and other phenylalanine-derived volatiles in tomato fruits and a small family of decarboxylases (LeAADC1A, LeAADC1B, and LeAADC2) that can mediate that pathway's first step. These enzymes each catalyze conversion of phenylalanine to phenethylamine and tyrosine to tyramine. Although tyrosine is the preferred substrate in vitro, phenylalanine levels in tomato fruits far exceed those of tyrosine, indicating that phenylalanine is a physiological substrate. Consistent with this view, overexpression of either LeAADC1A or LeAADC2 in transgenic tomato plants resulted in fruits with up to 10-fold increased emissions of the products of the pathway, including 2-phenylacetaldehyde, 2-phenylethanol, and 1-nitro-2-phenylethane. Further, antisense reduction of LeAADC2 significantly reduced emissions of these volatiles. Besides establishing a biosynthetic route, these results show that it is possible to change phenylalanine-based flavor and aroma volatiles in plants by manipulating expression of a single gene. metabolic engineering ͉ phenylalanine ͉ taste

Biosynthesis of plant‐derived flavor compounds

“…Formation of aldehyde (a) from amino acids requires the removal of both carboxyl and amino groups. The sequence of these removals is not fully known and could be the opposite to that shown or aldehyde could be formed in one step by aldehyde synthase (Kaminaga et al, 2006;Tieman et al, 2006). acid decarboxylase in tomato resulted in fruits with up to 10-fold increased levels of 2-phenylacetaldehyde, 2-phenylethanol and 1-nitro-2-phenylethane (Tieman et al, 2006).…”

“…Genes encoding enzymes responsible for the direct decarboxylation of phenylalanine have been isolated from tomato, petunia and rose, showing that alternative catabolic pathways exist in plants (Figure 9a) (Kaminaga et al, 2006;Tieman et al, 2006). Although the enzymes display subtle differences in sequences and enzymatic properties, their down-regulation led to reduced emission of 2-phenylacetaldehyde and 2-phenylethanol.…”

Alteration of the Interconversion of Pyruvate and Malate in the Plastid or Cytosol of Ripening Tomato Fruit Invokes Diverse Consequences on Sugar But Similar Effects on Cellular Organic Acid, Metabolism, and Transitory Starch Accumulation

“…They were subsequently extracted in 100% methanol and processed exactly as described (Timm et al, 2008). The metabolic fate of these substrates was subsequently assessed exactly as described previously (Tieman et al, 2006). A total of four biological replicates were used.…”

Enzyme Activity Profiles during Fruit Development in Tomato Cultivars andSolanum pennellii

“…In particular, a set of 76 near isogenic lines derived from an S. lycopersicum 'M82' 3 Solanum pennellii cross (Eshed and Zamir, 1994) has been subjected to extensive agronomic, physiological, and molecular phenotyping (Lippman et al, 2007). This has allowed quantitative trait loci (QTLs) to be detected that affect morphology and yield , fruit coloration (Liu et al, 2003), metabolite levels (Causse et al, 2004;Fridman et al, 2004;Baxter et al, 2005a;Schauer et al, 2006), volatile metabolites (Tieman et al, 2006), and antioxidants (Rousseaux et al, 2005). The cultivated tomato is one of the first examples of a crop plant that has benefited significantly from exotic germplasm introgression (Zamir, 2001;Lippman et al, 2007).…”

“…It has been used to study fruit shape and development (Causse et al, 2004;Brewer et al, 2007;Bertin et al, 2009), metabolite composition (Fridman et al, 2004;Tikunov et al, 2005;Schauer et al, 2006;Tieman et al, 2006;Bertin et al, 2009), flowering time (JimenezGomez et al, 2007), disease and fungus resistance (Chaerani et al, 2007;Finkers et al, 2007), tolerance to salinity (Cuartero et al, 2006;Villalta et al, 2007), and chilling (John Goodstal et al, 2005).…”