From Central to Specialized Metabolism: An Overview of Some Secondary Compounds Derived From the Primary Metabolism for Their Role in Conferring Nutritional and Organoleptic Characteristics to Fruit

Abstract

Fruit flavor and nutritional characteristics are key quality traits and ones of the main factors influencing consumer preference. Central carbon metabolism, also known as primary metabolism, contributes to the synthesis of intermediate compounds that act as precursors for plant secondary metabolism. Specific and specialized metabolic pathways that evolved from primary metabolism play a key role in the plant's interaction with its environment. In particular, secondary metabolites present in the fruit serve to increase its attractiveness to seed dispersers and to protect it against biotic and abiotic stresses. As a consequence, several important organoleptic characteristics, such as aroma, color, and fruit nutritional value, rely upon secondary metabolite content. Phenolic and terpenoid compounds are large and diverse classes of secondary metabolites that contribute to fruit quality and have their origin in primary metabolic pathways, while the delicate aroma of ripe fruits is formed by a unique combination of hundreds of volatiles that are derived from primary metabolites. In this review, we show that the manipulation of primary metabolism is a powerful tool to engineer quality traits in fruits, such as the phenolic, terpenoid, and volatile content. The enzymatic reactions responsible for the accumulation of primary precursors are bottlenecks in the transfer of metabolic flux from central to specialized metabolism and should be taken into account to increase the yield of the final products of the biosynthetic pathways. In addition, understanding the connection and regulation of the carbon flow between primary and secondary metabolism is a key factor for the development of fruit cultivars with enhanced organoleptic and nutritional traits.

Keywords: flavor; fruit; metabolic engineering; primary metabolism; quality traits; secondary metabolism.

Figure 1

(A) Flavonoid chemical structures, including the flavan nucleus and the main classes of flavonoids found in fruits. (B) Terpenoid chemical structures, including isoprene and an example of mono-(R-limonene), sesqui-(valencene), di-(phytol), tri-(oleanic acid), tetra-(β-carotene), and polyterpenoid (betulaprenole) compounds.

Figure 2

Overview of the shikimate pathway leading to the synthesis of phenolic acid compounds, including soluble (or hydrolysable) tannins, phenylpropanoids and phenylalanine-derived volatiles. Main classes of phenylpropanoids are shown in yellow. Primary pathways are indicated in blue, while secondary pathways are in red. Enzymes involved in the accumulation of primary metabolite precursors and possible targets for metabolic engineering are indicated in bold. Transcription factors involved in the regulation of carbon flux toward phenylpropanoid synthesis are shown in green (ODO1 from Petunia and MYB12 from Arabidopsis), and are located next to the pathways they controlled. PEP, phosphoenolpyruvate; DHAPS, 3-deoxy-d-arabino-heptulosonate 7-phosphate synthase; AroG, bacterial feedback insensitive DAHPS; PheA, bacterial feedback insensitive chorismate mutase/prephenate dehydratase; AADC, aromatic amino acid decarboxylase; ArAT, aromatic amino acid aminotransferase; PAL, phenylalanine ammonia lyase.

Figure 3

General overview of volatile and terpenoid compounds synthesis from pyruvate and acetyl-CoA. Enzymes involved in the accumulation of primary metabolite precursors and possible targets for metabolic engineering are indicated in bold. Primary pathways are indicated in blue; main classes of terpenoid compounds are shown in green, while volatile classes are emphasized in red. Pyr, pyruvate; PEP, phosphoenolpyruvate; BCAA, branched-chain amino acid; BCAT, branched-chain aminotransferase; ADH, alcohol dehydrogenase; AAT, alcohol aminotransferase; ACX, acyl-CoA oxidase; LIP1, lipase1; LOX, lipoxygenase; HPL, hydroperoxide lyase; DXS, 1-deoxy-D-xylulose 5-phosphate synthase; DXP, 1-deoxy-D-xylulose-5-phosphate; DXR, DXP reductoisomerase; MEP, 2-C-methyl-D-erythritol-4-phosphate; HMBPP, 1-hydroxy-2-methyl-2-(E)-butenyl 4-diphosphate; HDR, 1-hydroxy-2-methyl-2-(E)-butenyl 4-diphosphate reductase; IPP, isopentenyl diphosphate; DMAPP, dimethylallyl diphosphate; GPP, geranyl diphosphate: GGPS, GPP synthase; GGPP, geranylgeranyl diphosphate; GGPPS, geranylgeranyl diphosphate synthase; HMG-CoA, 3-hydroxy-3-methylglutaryl CoA; HMGR, 3-hydroxy-3-methylglutaryl CoA reductase; MVA, mevalonate.