Evolution of aromatic amino acid metabolism in plants: a key driving force behind plant chemical diversity in aromatic natural products

Abstract

A diverse array of plant aromatic compounds contributes to the tremendous chemical diversity in the plant kingdom that cannot be seen in microbes or animals. Such chemodiversity of aromatic natural products has emerged, occasionally in a lineage-specific manner, to adopt to challenging environmental niches, as various aromatic specialized metabolites play indispensable roles in plant development and stress responses (e.g. lignin, phytohormones, pigments and defence compounds). These aromatic natural products are synthesized from aromatic amino acids (AAAs), l-tyrosine, l-phenylalanine and l-tryptophan. While amino acid metabolism is generally assumed to be conserved between animals, microbes and plants, recent phylogenomic, biochemical and metabolomic studies have revealed the diversity of the AAA metabolism that supports efficient carbon allocation to downstream biosynthetic pathways of AAA-derived metabolites in plants. This review showcases the intra- and inter-kingdom diversification and origin of committed enzymes involved in plant AAA biosynthesis and catabolism and their potential application as genetic tools for plant metabolic engineering. I also discuss evolutionary trends in the diversification of plant AAA metabolism that expands the chemical diversity of AAA-derived aromatic natural products in plants. This article is part of the theme issue 'The evolution of plant metabolism'.

Keywords: aromatic amino acid; aromatic natural products; enzyme evolution; negative feedback inhibition.

Figure 1.

A pathway map and origin of the shikimate and aromatic amino acid biosynthetic pathways in plants. In plants, the shikimate pathway leads to the biosynthesis of AAAs, which are not only required for protein synthesis but also used as precursors of numerous AAA-derived aromatic natural products (yellow letters). The intermediates of the DHD-SDH and TS enzyme-catalysed reactions (3-dehydroshikimate and indole, respectively) are shown in brackets. Enzymes in the shikimate and AAA biosynthetic pathways are of mosaic origin, highlighted by purple (eukaryotic origin), green (cyanobacterial origin), magenta (α-proteobacterial origin) and blue (other prokaryotic origin). DHS, 3-deoxy-d-arabino-heptulosonate 7-phosphate (DAHP) synthase; DHQS, 3-dehydroquinate synthase; DHD-SDH, 3-dehydroquinate dehydratase-shikimate dehydrogenase; SK, shikimate kinase; EPSPS, 5-enolpyruvylshikimate 3-phosphate (EPSP) synthase; CS, chorismate synthase; AS, anthranilate synthase; PAT, phosphoribosylanthranilate transferase; PAI, phosphoribosylanthranilate isomerase; IGPS, indole-3-glycerol phosphate synthase; TSα, tryptophan synthase α subunit; TSβ, tryptophan synthase β subunit; CM, chorismate mutase; ADT, arogenate dehydratase; ADH, arogenate dehydrogenase; PPA-AT, prephenate aminotransferase; E4P, d-erythrose 4-phosphate; PEP, phosphoenolpyruvate and CdRP, 1-(o-carboxyphenylamino)-1-deoxy-ribulose 5-phosphate; EGT, endosymbiotic gene transfer; HGT, horizontal gene transfer.

Figure 2.

A model of plastidic and cytosolic post-chorismate pathways. Chorismate is exported from plastids through an unknown transporter and is branched to cytosolic Tyr and Phe biosynthetic pathways (left and right, respectively). A deregulated CM isoform converts chorismite into prephenate in the cytosol. Prephenate is subsequently dehydrogenased and dehydratased into HPP and phenylpyruvate by PDH and PDT enzymes that are insensitive to Tyr and Phe, respectively. HPP and phenylpyruvate are reversibly transaminated into Tyr and Phe, respectively. The contribution of cytosolic DHS enzymes to AAA metabolism in the cytosol remains unclear. DHS, 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase; CM, chorismate mutase; PDT, prephenate dehydratase; ADT, arogenate dehydratase; PDH, prephenate dehydrogenase; ADH, arogenate dehydrogenase; PPA-AT, prephenate aminotransferase; PPY-AT, phenylpyruvate aminotransferase; HPP-AT, 4-hydroxylphenylpyruvate aminotransferase; PAH, phenylalanine hydroxylase and HPP, 4-hydroxylphenylpyruvate.

Figure 3.

Feedback regulatory network in aromatic amino acid biosynthesis in plants. The pink lines with an arrowhead or a hash indicate known feedback activation or inhibition, respectively, while the dashed lines denote poorly characterized reactions or regulations that require further investigation. Blue or green colours indicate the reaction, enzyme and regulation that are known to be legume- or grass-specific, respectively. DHS, 3-deoxy-d-arabino-heptulosonate 7-phosphate synthase; AS, anthranilate synthase; CM, chorismate mutase; PDT, prephenate dehydratase; ADT, arogenate dehydratase; PDH, prephenate dehydrogenase; ADH, arogenate dehydrogenase; PPA-AT, prephenate aminotransferase; PPY-AT, phenylpyruvate aminotransferase; HPP-AT, 4-hydroxylphenylpyruvate aminotransferase; PAH, phenylalanine hydroxylase; PAL, phenylalanine ammonia-lyase; TAL, tyrosine ammonia-lyase; C4H, cinnamate 4-hydroxylase; E4P, d-erythrose 4-phosphate; PEP, phosphoenolpyruvate and HPP, 4-hydroxylphenylpyruvate.

Figure 4.

Trends in the diversification of aromatic amino acid metabolic enzymes. A single copy of an ancestral AAA metabolism gene is duplicated into multiple isoforms. Some of them are subsequently diversified to change their biochemical property, expression pattern and/or subcellular localization (magenta, orange and yellow, respectively). These divergent AAA metabolic enzymes probably play a critical role in optimized precursor supply for the biosynthesis of aromatic natural products. On the other hand, the isoform that is kept conserved to maintain the original functions (blue) probably contributes to basic amino acid homeostasis for protein synthesis.