Beyond brown: polyphenol oxidases as enzymes of plant specialized metabolism

Abstract

Most cloned and/or characterized plant polyphenol oxidases (PPOs) have catechol oxidase activity (i.e., they oxidize o-diphenols to o-quinones) and are localized or predicted to be localized to plastids. As a class, they have broad substrate specificity and are associated with browning of produce and other plant materials. Because PPOs are often induced by wounding or pathogen attack, they are most generally believed to play important roles in plant defense responses. However, a few well-characterized PPOs appear to have very specific roles in the biosynthesis of specialized metabolites via both tyrosinase (monophenol oxidase) and catechol oxidase activities. Here we detail a few examples of these and explore the possibility that there may be many more "biosynthetic" PPOs.

Keywords: 8-8’ linked lignans; L-DOPA; aurones; betalains; metabolism; specialized metabolism; tyramine; tyrosine.

FIGURE 1

Involvement of polyphenol oxidases (PPOs) in plant specialized metabolism. Steps where PPO involvement has been demonstrated or proposed are highlighted in red. For simplicity, not all reactants, enzymes, or stereochemistry are shown. Steps that occur spontaneously (not mediated by an enzyme) are indicated. (A) Betalain synthesis as described by Hatlestad et al. (2012), Gandia-Herrero and Garcia-Carmona (2013), and others. DODA, DOPA 4,5-dioxygenase; CYP76AD1, the cytochrome P450 described by Hatlestad et al. (2012). The reaction mediated by CYP76AD1 likely proceeds via a DOPA quinone intermediate (Gandia-Herrero and Garcia-Carmona, 2013). (B) Proposed tyrosine metabolism in walnut (Araji et al., 2014). Values in parentheses are fold change in metabolite in walnut plants with PPO silenced via RNAi relative to wild type control plants as reported by Araji et al. (2014). Tyrosine levels did not change and L-DOPA itself was not detectable. (C) 3,3′-Dihydroxylarreatricin biosynthesis in creosote bush as proposed by Cho et al. (2003). L3′H, larreatricin 3′-hydroxylase. (D) (i) Aureusidin biosynthesis in A. majus as proposed by Nakayama et al. (2001). AS, aureusidin synthase (here, a vacuolar PPO); THC, 2′,4′,6′,4-tetrahydroxychalcone; PHC, 2′,4′,6′,3,4-pentahydroxychalcone. For simplicity, bracteatin formation from PHC by AS is not shown. (ii) Sulfuretin biosynthesis in C. grandiflora as proposed by Kaintz et al. (2014). AS, aurone synthase (here, a plastidic PPO).