Primary Metabolism in Citrus Fruit as Affected by Its Unique Structure

Abstract

Citrus is one of the world's most important fruit crops, contributing essential nutrients, such as vitamin C and minerals, to the human diet. It is characterized by two important traits: first, its major edible part is composed of juice sacs, a unique structure among fruit, and second, relatively high levels of citric acid are accumulated in the vacuole of the juice sac cell. Although the major routes of primary metabolism are generally the same in citrus fruit and other plant systems, the fruit's unique structural features challenge our understanding of carbon flow into the fruit and its movement through all of its parts. In fact, acid metabolism and accumulation have only been summarized in a few reviews. Here we present a comprehensive view of sugar, acid and amino acid metabolism and their connections within the fruit, all in relation to the fruit's unique structure.

Keywords: acidity; amino acids; citrate; citrus fruit; primary metabolism; quality; sugars.

Figure 1

Citrus fruit morphology. Cross section of the fruit (A), and schematic representation of a segment, including the peel tissues (B). The segment epidermis also covers the juice sacs, and the three segment vascular bundles — dorsal and two septal — do not reach the pulp tissues.

Figure 2

Sugar metabolism and the interconversion of fructose-6-phosphate to fructose-1,6-bisphosphate (shaded). Compound inhibiting (red triangle) or inducing (green triangle) the activities of FBPase, PFP and PFK are shown. INV, invertase; SUSY, sucrose synthase; SPS, sucrose phosphate synthase; SPP, sucrose phosphate phosphatase; HK, hexose kinase; FK, fructokinase; UDPGluPho, UDP glucose phosphatase; PhoGluMu, phosphoglucose mutase; PhHexIso, phosphohexose isomerase; FBPase, fructose bisphosphate phosphatase; PFP, pyrophosphate-dependent fructose 6-phosphate kinase; PFK, ATP-dependent fructose 6-phosphate kinase; Fru-2,6-P₂, fructose-2,6, bisphosphate; 2OG, 2-oxoglutarate.

Figure 3

Possible mechanism of sugar transport and metabolism in citrus fruit. Schematic presentation showing the possible paths of sucrose movement and hydrolysis in the various fruit tissues. Suc, sucrose; Glu, glucose; Fru, fructose; UDP-Glu, UDP glucose; V, vacuole; SUSY, sucrose synthase; VINV, vacuolar invertase; CWINV, cell-wall invertase; CINV, cytosolic invertase; plasmodesmata.

Figure 4

Glycolysis, tricarboxylic acid metabolism, their metabolic connections to amino acids, and citrate and pH homeosthasis in the juice sac cell. The GABA shunt connecting glutamate and 2-oxoglutarate (I), the V-type H⁺-ATPAse (II), the H⁺-pyrophosphatase (III) and the Citrate/H⁺ symporter (IV) are shaded. H⁺/ATP coupling ratio and its pH dependence are indicated. ΔpH (yellow triangle) across the tonoplast is generated by the activities of the H⁺-ATPase and the H⁺-PPiase, and is induced by Mg⁺² and reduced by BAF and nitrate. V-ATPase is inhibited by bafilomycin (BAF) and nitrate. The Citrate/H⁺ symporter is driven by the acidification of the vacuole (pH decrease). The relative distribution of the various forms of citrate under different vacuolar pH values are shown in the inset figure, as explained in the text. Fru-1,6biP, fructose 1,6-bisphosphatase; DiHOAcP, dihydroxyacetone phosphate; 3-PGIAld, 3-phosphoglyceraldehyde; 1,2-diPGA, 1,2-diphosphoglycerate; 3-PGA, 3-phosphoglyceric acid; 2-PGA, 2-phosphoglyceric acid; PEP, phosphoenolpyruvate; Pyr, pyruvate; Ac-CoA, acetyl-Coenzyme A; 2-OXG, 2-oxoglutarate; Succ-CoA, succinyl-coenzyme A; OAA, oxaloacetate; 2OX, 2-oxoglutarate; GABA, γ‐aminobutyric acid; SSA, succinic semialdehyde; PGlyMut, phosphoglycerate mutase; PyrKin, pyruvate kinase; PyrDehyd, pyruvate Dehydrogenase; CS, citrate synthase; IDH, isocitrate dehydrogenase; 2-OGDehyd, 2-oxoglutarate dehydrogenase; Succ-CoA Syn, succinyl-CoA synthase; SuccDehyd, succinate dehydrogenase; MalDehyd, malate dehydrogenase; PEPCar/Kin, phosphoenolpyruvate carboxykinase; GOT, glucooxaloacetate transaminase; GPT, glucopyruvate transaminase; GOGAT, glutamine oxoglutarate aminotransferase; GS, glutamine Synthetase; GAD, glutamate decarboxylase; GABAT,4-aminobutyrate-2-ketoglutarate transaminase; SSADH, succinic semialdehyde dehydrogenase.