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Try out PMC Labs and tell us what you think. Learn More. In contrast to the detailed molecular knowledge available on anthocyanin synthesis, little is known about its catabolism in plants. Litchi Litchi chinensis fruit lose their attractive red color soon after harvest.

The mechanism leading to quick degradation of anthocyanins in the pericarp is not well understood. An anthocyanin degradation enzyme ADE was purified to homogeneity by sequential column chromatography, using partially purified anthocyanins from litchi pericarp as a substrate. The anthocyanin degradation function of the gene was confirmed by its transient expression in tobacco Nicotiana benthamiana leaves.

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This model was supported by a dramatic decrease in epicatechin content in the pericarp parallel to anthocyanin degradation. Anthocyanins are one of the most abundant pigments in the plant kingdom, responsible for red, purple, and blue colors of flowers, fruits, and seeds. They play a central role in attracting pollinators and seed dispersers, as well as protecting plant tissues from biotic and environmental stress factors. Anthocyanin content in plants is dependent on the rate of their synthesis, their stability in the vacuoles, and the rate at which they are degraded.

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In contrast to the detailed molecular knowledge available on anthocyanin synthesis, there is little information on the catabolic pathway of anthocyanins in plants Oren-Shamir, Numerous color-changing phenomena in plants, which occur in different tissues and during diverse plant development processes, were found to be related to anthocyanin degradation Oren-Shamir, Anthocyanins are often produced to protect young leaves, and are degraded as the leaves mature Steyn et al.

Anthocyanin accumulation is ificantly induced in plants under stress conditions, such as high light intensity, low temperature, drought, or nutrition deficiency, and is degraded once the stress is eliminated Winkel-Shirley, ; Rowan et al. Rapid anthocyanin degradation occurs in Brunfelsia calycina yesterday-today-tomorrow petals after flower opening Zenner and Bopp, ; Vaknin et al. Anthocyanins are degraded during pear fruit maturity Pyrus communis ; Steyn et al. Additional examples of reduced anthocyanin concentrations occur during the development of grape berries Mori et al.

In vivo anthocyanin degradation was investigated mainly in fruits and ornamentals, in which preserving the pigmentation is crucial for maintaining high quality of the produce. These studies are based on the knowledge accumulated from pigment loss in fruit juices and wines Cheynier et al. Polyphenol oxidases PPOs and peroxidase POD are the main enzymes that oxidize anthocyanins in fruit extracts, Tennessee essentials date and litchi review to the decrease in pigment content Sarni et al. Active enzymatic anthocyanin degradation dependent on novel mRNA and protein biosynthesis was demonstrated in B.

Recently, a basic peroxidase, BcPrx01, was found to be responsible for the in planta degradation of anthocyanins in B. BcPrx01 has the ability to degrade complex anthocyanins. It colocalizes with these pigments in the vacuoles of petals, and both the mRNA and protein levels of BcPrx01 are greatly induced parallel to the degradation of anthocyanins. Litchi is a tropical and subtropical fruit of high commercial value.

The white translucent aril and attractive red color due to high content of anthocyanins in the pericarp contribute ificantly to their value. Revealing the anthocyanin degradation pathway during pericarp browning may help preserve the original red coloration of the fruit pericarp. Postharvest browning of fruits and vegetables has long been considered a function of PPO, catalyzing the oxidation of an array of aromatic substrates resulting in brown colored by-products.

The activity of PPO on exogenous substrates, such as catechol and 4-methylcatechol, was confirmed in litchi pericarp Jiang and Fu, ; Sun et al. However, the purified PPO from litchi pericarp could oxidize anthocyanins only in the presence of exogenous catechol Jiang, ; Zhang et al. This process is known as the anthocyanin-PPO-phenol model Kader et al. The question still remains whether this is the process occurring in vivo in litchi pericarp.

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Here, we describe the enzymatic process by which anthocyanins are degraded in litchi pericarp. The anthocyanin degradation enzyme ADE was purified to homogeneity and identified as a laccase LACbased on protein sequencing, gene cloning, and antibody verification.

Pericarp browning began 2 d after harvest, and by 4 d, the characteristic red pigmentation disappeared. When partially purified pericarp anthocyanins were incubated with a crude pericarp protein extract, the pigments turned brown within 10 min.

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This decoloration was due to ADE activity, since the anthocyanins remained red when incubated with the denatured enzyme extract Fig. The rate of ADE activity in the harvested pericarp was 0. Anthocyanin degradation and ADE activity during the browning of litchi fruit after harvest. Change in fruit color A and anthocyanin contents B was recorded during fruit browning. C, Browning of litchi anthocyanin due to the ADE activity in the crude pericarp enzyme extract, with the denatured enzyme extract De-ADE as a reference.

D, The time course of pericarp ADE activity during fruit browning. The values presented in C and D are means of three measurements from three individual extractions.

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Error bars indicate the sd of the values. The eluted fractions with high ADE activity in the first activity peak sample nos. Fractions from the major activity peak with high activity sample nos. Purification of the ADE from litchi pericarp. A, Total protein nm and ADE activity determined in DEAE-Sepharose chromatography fractions from pericarp crude enzyme extract, after ammonium sulfate fractionation.

Enzyme activities of pooled and nonpooled fractions, the Aand the NaCl gradients for A and B are indicated. E, In-gel activity assay of the purified ADE after Sephadex G chromatography with partially purified litchi anthocyanins as substrates. To further confirm that the purified protein contains ADE activity, the fraction was run on an activity gel.

A single brown band of kD was detected 4 min after incubating the gel in the litchi anthocyanin substrate, indicating ADE activity Fig. A purple-magenta color was seen on this protein band after staining with periodic acid-Schiff, suggesting that this ADE protein is a glycoprotein Fig. Four peptides with high similarity to published protein sequences were identified Table I.

The purified ADE efficiently oxidized several o -diphenols, such as epicatechin, catechol, and 4-methyl catechol, as well as hydroquinone a p -diphenoltwo monolignols coniferyl alcohol and sinapyl alcoholand ABTS a universal laccase substratestrongly indicating the ADE is a laccase.

This is the first report in which epicatechin was included in the substrate specificity analysis for laccases or PPOs. Overlapping absorbance spectra at nm were found for epicatechin and its oxidation product, and an obvious increase at nm was observed after the reaction was initiated by the addition of the purified ADE Supplemental Fig. Hydroquinone was the least favored substrate Table II. Both phloroglucinol and p -anisidine were not oxidized by the purified ADE.

The great difference in activity between the highly and partially purified anthocyanins suggests that certain endogenous substrates for the enzyme exist in the partially purified pigment necessary for the reaction to take place. An mRNA sequence of 1. The CDS encoded a protein of amino acids and a molecular mass of around 62 kD. The difference in migration of the corresponding protein on SDS- may be due to the existence of carbohydrate moieties detected on the purified protein band Fig.

Several N -glycosylation sites are present in the deduced amino acid sequence Fig. A secretion pathway protein al was detected at the N terminus Fig. Based on the 3D model of a fungal laccase Protein Data Bank code no.

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The following sequences from NCBI were used: 1 highly identical laccases; 2 extensively studied laccases A. The gene bank accession s for the correspondent mRNA sequences coding the enzymes are presented. B, The deduced amino acid sequence. Peptides used for antibody production are underlined. The arrangement of the domain structure is depicted with similar colors as in B. The in-gel activities were assayed as described in Figure 2 D with partially purified litchi anthocyanins for ADE substrate and 1,8-diaminonaphthalene DAN for laccase substrate.

The details of the values presented in C are as described in Figure 1. The molecular masses of these proteins were around kD, slightly less in comparison with the native protein from litchi pericarp. Furthermore, the in-gel activities using partially purified litchi anthocyanins as substrate also correlated with the above protein and transcript levels Fig. When using DANa universal substrate for phenol oxidase, higher activity levels were detected in the root and pericarp in comparison with other tissues Fig. The correlated patterns of the transcript, protein, and activity levels confirm that the litchi ADE is indeed a laccase, with high expression levels in the pericarp.

High expression levels of this enzyme in the pericarp are in correlation with the rapid anthocyanin degradation and browning occurring in this tissue after harvest.

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The effect of several inhibitors for PPOs and laccases was tested on the ADE activity in the crude litchi pericarp protein extract. When litchi fruit pericarp sections were incubated with artificial laccase substrates, the cells in the mesocarp closest to the epicarp acquired a distinct red-brown or brown color Fig. No color change was observed in controls that did not contain a substrate Fig. In most cells, the brown coloration was present in both the intracellular and extracellular spaces. A, Cross-sections of litchi pericarp incubated with 4-methylcatechol resulted in a red-brown coloration in the mesocarp.

D, Boiled control gave no coloration. M, Mesocarp; ep, epicarp.

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Some YFP fluorescence was detected at the boundary of Lysotracker red-stained vacuoles, and some was inside the vacuoles of a plasmolyed epidermal cell E and F.