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. 2020 Nov 18;10:20017. doi: 10.1038/s41598-020-75636-y

Comprehensive ESI-Q TRAP-MS/MS based characterization of metabolome of two mango (Mangifera indica L) cultivars from China

Lin Tan 1, Zhiqiang Jin 2, Yu Ge 1, Habibullah Nadeem 3, Zhihao Cheng 1, Farrukh Azeem 1,3,✉, Rulin Zhan 1,✉
PMCID: PMC7676270  PMID: 33208758

Abstract

Polyphenols based bioactive compounds from vegetables and fruits are known for impressive antioxidant activity. Ingestion of these antioxidants may promote human health against cardiovascular diseases and cancer. Mango is a popular tropical fruit with special taste, high nutritional value and health-enhancing metabolites. The aim was to investigate the diversity of phytochemicals between two mango cultivars of china at three stages of fruit maturity. We used ESI-QTRAP-MS/MS approach to characterize comprehensively the metabolome of two mango cultivars named Hongguifei (HGF) and Tainong (TN). HPLC was used to quantify selected catechin based phenolic compounds. Moreover, real-time qPCR was used to study the expression profiles of two key genes (ANR and LAR) involved in proanthocyanidin biosynthesis from catechins and derivatives. A total of 651 metabolites were identified, which include at least 257 phenolic compounds. Higher number of metabolites were differentially modulated in peel as compared to pulp. Overall, the relative quantities of amino acids, carbohydrates, organic acids, and other metabolites were increased in the pulp of TN cultivar. While the contents of phenolic compounds were relatively higher in HGF cultivar. Moreover, HPLC based quantification of catechin and derivatives exhibited cultivar specific variations. The ANR and LAR genes exhibited an opposite expression profile in both cultivars. Current study is the first report of numerous metabolites including catechin-based derivatives in mango fruit. These findings open novel possibilities for the use of mango as a source of bioactive compounds.

Subject terms: Plant sciences, Plant molecular biology

Introduction

Fruits of tropical and subtropical regions are appreciated as energy suppliers, as well as for the presence of health-enhancing metabolites. Plant origin secondary metabolites are the focus of research for numerous health-beneficial properties and antioxidant activities. Mango (Mangifera indica (L.) Lam.) is an important tropical fruit and rank fifth in global production (55.6 million tonnes/year) after banana, apple, grapes, and oranges1. Numerous cultivars of mango are found worldwide, which show variations in fruit peel color, size, shape, and composition2,3. Apart from being consumed fresh, mangoes are also used to make desserts, juices, pickles, marmalades and jam4. During processing, a significant portion of the fruit is removed, which generates millions of tons of mango waste every year. However, the peel of mango fruit may be interesting for the presence of high levels of health-promoting compounds2,4. It seems in line with the efforts to explore the cost-effective potential of agri-waste for industrial use or to reduce its negative effects on the environment. The identification and reclamation of important metabolites from mango or its byproducts is a difficult task and its completion would promote the revaluation of mango as a natural source of antioxidants/bioactive compounds. In this regard, large scale metabolite profiling seems a promising way to explore metabolite potential of mango fruit.

Proanthocyanidins (PAs) are oligo/polymeric flavonoids that are naturally present in many vegetables, nuts, seeds and fruits5. Flavan-3-ols constitute the structural units of PAs and consist of C6-C3-C6 based flavonoid skeleton. There are two most common forms of these metabolites as 2,3-cis-(–)-epicatechin and 2,3-trans-(+)-catechin6. Flavan-3-ols (as monomers or as PAs) promote plant resistance against various biotic and abiotic stresses7. These metabolites possess numerous pharmacological properties, hence involved in scavenging free radicals, antimicrobial, antioxidant, anti-nutritional, anti-cancer and cardiac protection activities8,9. Quantitative and qualitative differences in the phytochemical profiles of mango cultivars may contribute to distinguishing their health-promoting properties.

The biochemical composition of fruits (sugars, organic acids, flavonoids, etc.) predominantly influences the consumer preference for visual features and taste. Several researchers have investigated the nutritional composition of mangoes10–12. However, very limited information is available about the identities of metabolites, which govern important properties of this fruit. In addition, there is a lack of studies for comprehensive identification, documentation, and quantification of flavonoids and other secondary metabolites. Instead of thoroughly evaluating all of the phytochemicals, researchers have attempted to study only particular metabolites of mango10,13,14. Recent advancements in widely-targeted metabolomics (supported by techniques like LC–MS/MS) have made possible a prompt and ultra-sensitive detection of a huge number of metabolites15,16. The liquid chromatography-tandem mass spectrometry is employed in the current study to identify and detect relative quantities of metabolites from two mango cultivars exhibiting contrasting features in terms of shape, size, taste and peel color2. This study aims at the revelation of the metabolic variations between two mango cultivars (from China) with distinct features2,17 and offers valuable data for appraising its nutritional importance in industrial utilization and breeding strategies.

Results and discussion

Metabolic profiling

Previous studies have reported the quantification of individual metabolite classes in mango pulp and peel10,18–24. In most of these studies, a standard metabolite was used to identify an exact compound or a relevant group of metabolites. However, based on these studies it was difficult to envisage comprehensive metabolic dynamics in mango. In current study, a total of 651 metabolites were annotated/ identified in three growth stages (Table S1), which include 54 nucleotides and their derivatives; 21 carbohydrates and their derivatives; 99 amino acids and their derivatives; 67 lipids and their derivatives; 6 indole derivatives; 8 alcohols and polyols; 2 terpenoids; 5 alkaloids; 21 vitamins and their derivatives; 72 organic acids; 257 phenolic compounds and 38 other metabolites.

Principal component analysis (PCA) for metabolite profiles

To assess relative variations in metabolic profiles (for 651 metabolites), we used multivariate statistics. Hierarchical cluster analysis (HCA), for relative differences in accumulation patterns at three growth stages, arranged metabolites from both cultivars into three groups (Fig. 1A). Peel and pulp samples exhibit distinct metabolite profiles in terms of upregulated or downregulated compounds in a cultivar and growth stage-specific manner (Fig. 1A, Table S2). The metabolites in peel at stages 1 and 2 are clustered in the same column as compared to third stage metabolites. On the other hand, metabolites at stages 2 and 3 are clustered in a similar column for pulp samples as compared to the first stage. It suggests the diversity of metabolites in peel samples at the third stage of fruit growth.

Figure 1.

Figure 1

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HCA and PCA analysis of relative metabolite variations in peel and pulp samples of both cultivars. Both the HCA and PCA analysis was performed using all the metabolites annotated in current study. (A) Heat map for HCA. An online tool (heatmapper)25 was used to visualize the metabolite variations. The complete linkage hierarchical clustering was used for normalization. Each column represents a pairwise comparison of metabolites from both cultivars at a particular stage, while each row represents a metabolite. The red color is an indication of a higher concentration in HGF and green color represents a higher concentration of the metabolite in TN. (B) PC1 and PC2 score plots for pulp and peel between both cultivars. TN1, TN2, TN3, HGF1, HGF2, and HGF3 represent pulp samples of TN and HGF cultivars at first, second and third stage respectively. Similarly, TNS1, TNS2, TNS3, HGFS1, HGFS2, and HGFS3 represent peel samples of TN and HGF cultivars at first, second and third stage respectively. QC, mix represents quality control samples.

PCA is extensively applied in chemometric experiments to extract and rationalize important facts from biological systems with multivariate descriptions. By using this analysis, we can determine the core arrangement of variables in terms of principal components. According to PCA plots (Fig. 1B), the QC samples (mix) formed a close cluster, which indicates the similarity of metabolic profiles and stability/repeatability of analysis. Consistently, based on the PC1, a clear separation could be observed between the peel and pulp metabolites. Additionally, both cultivars are clearly distinguished by PC2 (Fig. 1B). This finding suggests the existence of distinct metabolic programs in peels and pulps. Moreover, both cultivars exhibit discrete metabolites in respective tissues that could be the basis of their contrasting features.

Partial least-squares discriminant analysis (PLS-DA) for differential metabolites

For the estimation of potential contributions of metabolites in cultivar-specific features, pairwise comparisons were performed using OPLS-DA models among three stages of mango fruit for pulp and peel (as inter-cultivar pairs). As a result, higher predictability (Q2) and strong goodness of fit (R2X, R2Y) were observed for these models. (Table S3; Fig. S1). All the values of R2X, R2Y and Q2 in OPLS-DA are above 0.7 and even many of them are close to 1 (Table S3), indicating the models is very good. Besides, R2Y in the permutation test of OPLS-DA of each group is very close to 1 (Fig. S1), suggesting the established model conforms to the real situation of sample data. The Q2 in each model is very close to 1, which shows that the model can well explain the difference between the two groups of samples. The model has no over fitting phenomenon and is very stable. For further improving our understanding of metabolic variations, we performed a differential metabolite screening among all detected metabolites for fold-change and the projection scores or VIP values. The metabolites were considered differentially expressed if the p value was less than 0.05 and the VIP value was greater than 1. The results of this screening are presented using Volcano plots in Fig. 2A and summarized in Table S2.

Figure 2.

Figure 2

Figure 2

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Volcano plots and Ven diagrams for differentially expressed metabolites in peel and pulp samples. (A) volcano plots; (B) Ven diagram of pulp samples; (C) Ven diagram of peel samples. TN1, TN2, TN3, HGF1, HGF2, and HGF3 represent pulp samples of TN and HGF cultivars at first, second and third stage respectively. Similarly, TNS1, TNS2, TNS3, HGFS1, HGFS2, and HGFS3 represent peel samples of TN and HGF cultivars at first, second and third stage respectively.

To study the cultivar-specific relative quantification of metabolites in the pulp, a comparison was drawn between pulp metabolites of HGF and TN cultivars. At 1st stage of fruit growth, there were 231 differential metabolites (87 and 144 up-regulated in HGF and TN, respectively), 252 metabolites (47 and 205 up-regulated in HGF and TN, respectively) at 2nd stage, and 261 metabolites (76 and 185 up-regulated in HGF and TN, respectively) at 3rd stage (Fig. 2B, HGF1-TN1, HGF2-TN2, HGF3-TN3). In other words, a higher number of metabolites were up-regulated in TN cultivar as compared to HGF.

Metabolites in pulps

To address the prospective importance of metabolite concentration in fruit maturity features, it was observed that sebacate and ρ-hydroxyphenyl acetic acid (organic acids); indole and epigallocatechin (catechin derivative) were present in very high amounts (> 10 log_fold) in TN pulp (Table S2, represented by blue color in HGF3-TN3). On the other hand in HGF cultivar, 6-hydroxynicotinic acid (vitamins); rosinidin o-hexoside (Anthocyanins); protocatechuic aldehyde (catechin derivatives); syringic acid, 1-o-beta-d-glucopyranosyl sinapate (hydroxycinnamoyl derivatives); chrysin o-hexoside, chrysin 5-o-glucoside (toringin) (flavone); o-feruloyl quinic acid (quinate and its derivatives); eriodictyol c-hexoside (flavone c-glycosides); and aromadedrin (flavonol) were present in very high amounts (> 10 log_fold). Overall, the relative quantities of amino acids, carbohydrates, organic acids, and other metabolites were higher in the pulp of TN cultivars. While the contents of phenolic compounds were relatively higher in HGF cultivar. It explains better sweetness/taste of TN and better quality of HGF pulp17. Among others, syringetin (a flavonol) was detected only at the 2nd stage as ~ 10.71 log_fold higher contents in HGF as compared to TN. This compound has never been reported in mango. Besides, it was just reported in grape and wine26. This metabolite can induce human osteoblast differentiation through bone morphogenetic protein‐2/extracellular signal‐regulated kinase 1/2 pathway26. It can also enhance radio-sensitivity more effectively in cancer cells than in normal cells through enhancement of the caspase-3-mediated apoptosis pathway27. Moreover, growth stage or cultivar-specific variations in metabolite contents may provide important information in identifying respective molecular markers for mango fruit selection at different growth stages (Fig. 2B).

Metabolites in peels

In a comparison of peel samples between HGF and TN cultivars, the upregulated metabolites were as follows: 357 at 1st stage (165 HGF vs 192 TN), 379 at 2nd (138 HGF vs 241 TN) and 375 at 3rd (136 HGF vs 239 TN) (Fig. 2C). However, in the comparison of differential metabolites between growth stages, a higher number of metabolites were upregulated in lateral growth stages. Likewise pulp metabolites, TN peel exhibited up-regulation of a higher number of metabolites as compared to peel of HGF (Fig. 2C).

With a view to exploit the potential of mango peel as a source of valuable metabolites that vary between these two cultivars at very high levels (> 13 log_fold), following metabolites were detected in HGF peel (as compared to TN): DIMBOA glucoside (cyclic hydroxamic acid); spinacetin (flavone); sissotrin (isoflavone); C-hexosyl-chrysoeriol o-hexoside (flavone C-glycosides); cucurbitacin D (terpenoids); gentisic acid (benzoic acid derivatives); Vanillic acid (hydroxycinnamoyl derivatives); N-sinapoyl hydroxycoumarin (coumarins) (Table S2, HGFS3-TNS3). These metabolites mainly constituted flavonoids and may be considered as representative differential metabolites for the different peel colors in both cultivars (Table S2). DIMBOA glucoside represented the most upregulated compound in the peel of HGF cultivar (> 15 log_fold). It belongs to benzoxazinoids (a group of cyclic hydroxamic acids), which are found prevalently in the members of family Poaceae. This metabolite has been reported from Secale cereale L., Triticum aestivum L. and Zea mays L.28. The benzoxazinoid derivatives were discovered in nature in the 1950s and have been attracting significant scientific interest in nutrition and pharmaceutics during the past decade29. Benzoxazinoid hydroxamic acids have been reported that exhibit phytotoxic activities, playing a significant role in plant defense against fungi, bacteria, insects, and participating in allelopathy mechanisms28,30. In this context, it is the first report of DIMBOA-glucoside outside the grass family. Similarly, cucurbitacins are identified as tetracyclic triterpenoids and belong to the Cucurbitaceae family. They are known to have diverse pharmacological activities including antimicrobial activities, anti-inflammatory, antitumor and cardiovascular properties31. Cucurbitacin D (Table S2, HGFS3-TNS3; > 13 log_fold) effectively inhibits glucose uptake and lactate production in metastatic prostate cancer cells via modulating glucose metabolism32. These findings open novel possibilities for the use of mango peel as a source of plant bioactive compounds.

Differential metabolic pathways

To obtain detailed pathway information, the Kyoto Encyclopedia of Genes and Genomes (KEGG) database (https://www.genome.jp/kegg/) was used to map the differential metabolites between both cultivars (Fig. S2, Table S4). The identified metabolic pathways with differential metabolites compared between pulps or peels of both cultivars are shown in Fig. S2A and S2B. These pathways were mainly involved in aminoacyl-tRNA biosynthesis, purine metabolism, glucosinolate biosynthesis, phenylpropanoid biosynthesis (PP), flavonoid biosynthesis and pathways involved in amino acid metabolism (Table S4). These pathways are also involved in the metabolism of plant secondary metabolites. Flavonoids are considered one of the major contributors to crucial features of fruits. The PP pathway in pulp and peel samples differed between both cultivars for differentially expressed metabolites (DEMs) (Fig. S2A and S2B). It is possible that the expression of flavonoid biosynthesis-related genes could be related to genotypic differences.

Phenolic compounds

As the phenolic compounds constituted the largest group of metabolites identified in this analysis, so we decided to analyze this group in detail (Table 1). Previously, a variable but limited number of phenolic compounds were reported in mango fruit10,19,33. Mango fruit generally contains two groups of phenolic acids i.e., hydroxybenzoic and hydroxycinnamic acid derivatives. In literature, hydroxybenzoic acids like protocatechuic acid, vanillic acid, ρ-hydroxybenzoic acid, gallic acid, syringic acid and hydroxycinnamic acids like caffeic acid, chlorogenic acid, ferulic acid, and ρ-coumaric acid have been reported in mango. Although, the metabolic content and type vary with geographical location, plant age and variety2. In current study, the majority of metabolites are reported for the first time in mango (Table 1).

Table 1.

All the phenolic compounds identified in mango fruit (pulp and peel) of both cultivars during three growth stages.

Sr. no Class Metabolite Precursor ions Q1 (Da) Product ions Q3 (Da) Rt. (min) Molecular weight (Da) Ionization model KEGG.ID
1 Anthocyanins Cyanidin 3-O-glucosyl-malonylglucoside 697.1 696.9 2.24 697.1 [M+H]+ –
2 Anthocyanins Delphinidin 3-O-glucoside (Mirtillin) 465.1 303.1 2.26 465.1 [M+H]+ C12138
3 Anthocyanins Pelargonin 595 271.8 2.38 595 [M+H]+ C08725
4 Anthocyanins Petunidin 3-O-glucoside 479 317 2.56 479 [M+H]+ C12139
5 Anthocyanins Cyanidin 3-O-glucoside (Kuromanin) 449.1 287.3 2.59 449.1 [M+H]+ C08604
6 Anthocyanins Cyanidin O-syringic acid 465.1 285.3 2.59 466.1 [M−H]− –
7 Anthocyanins Pelargonidin 3-O-β-D-glucoside (Callistephin chloride) 433.1 271 2.83 433.1 [M+H]+ –
8 Anthocyanins Malvidin 3-O-glucoside (Oenin) 493.2 331.6 2.92 493.2 [M+H]+ C12140
9 Anthocyanins Delphinidin 303 149.3 2.98 303.24 [M+H]+ C05908
10 Anthocyanins Peonidin O-malonylhexoside 547.1 503.4 3 548.1 [M−H]− –
11 Anthocyanins Cyanidin O-diacetyl-hexoside-O-glyceric acid 619.1 531.3 3.26 620.1 [M−H]− –
12 Anthocyanins Rosinidin O-hexoside 477.1 315.6 3.32 477.1 [M+H]+ –
13 Anthocyanins Cyanidin 287 231.6 3.54 287.24 [M+H]+ C05905
14 Anthocyanins Pelargonidin 271 215.1 3.85 271.24 [M+H]+ C05904
15 Anthocyanins Peonidin 301.1 273.6 3.95 301.1 [M+H]+ C08726
16 Benzoic acid derivatives Anthranilate O-hexosyl-O-hexoside 460.1 118.2 0.78 461.1 [M−H]− –
17 Benzoic acid derivatives Gallic acid 169 122.8 1.74 170.022 [M−H]− C01424
18 Benzoic acid derivatives 2,5-dihydroxy benzoic acid O-hexside 315.1 152.1 1.84 316.1 [M−H]− –
19 Benzoic acid derivatives Gallic acid O-Hexoside 331 313.7 2.02 332 [M−H]− –
20 Benzoic acid derivatives Syringic acid O-glucoside 359.1 197.1 2.26 360.1 [M−H]− –
21 Benzoic acid derivatives 2,5-dihydroxybenzoic acid (Gentisic acid) 153 108.1 2.5 154.027 [M−H]− C00628
22 Benzoic acid derivatives 2,4-Dihydroxybenzoic acid 153 109 2.75 154.027 [M−H]− –
23 Benzoic acid derivatives Methyl gallate 183 124.1 3.14 184.0372 [M−H]− –
24 Benzoic acid derivatives p-Aminobenzoate 137.3 94.3 3.14 136.3 [M+H]+ C00568
25 Benzoic acid derivatives 4-Hydroxybenzaldehyde 121 91.9 3.72 122.037 [M−H]− C00633
26 Benzoic acid derivatives Ethyl gallate 197.1 124.1 3.87 198.0528 [M−H]− –
27 Benzoic acid derivatives Vanillin 151 136.1 4 152.0473 [M−H]− C00755
28 Benzoic acid derivatives 8-Methyl-2-oxo-4-phenyl-2H-chromen-7-yl 4-(hexyloxy)benzoate 457.2 191.5 4.48 456.2 [M+H]+ –
29 Benzoic acid derivatives Benzoic acid 121 77 4.57 122.0368 [M−H]− C00180
30 Catechin derivatives ( +)-Gallocatechin (GC) 307 248.1 2.27 306.074 [M+H]+ C12127
31 Catechin derivatives Protocatechuic acid O-glucoside 315.1 153.2 2.44 316.1 [M−H]− –
32 Catechin derivatives Protocatechuic acid 153.1 109.1 2.48 154.027 [M−H]− C00230
33 Catechin derivatives Epigallocatechin (EGC) 307 139.1 2.73 306 [M+H]+ C12136
34 Catechin derivatives Epigallocatechin (EGC) 305 125 2.76 306 [M−H]− C12136
35 Catechin derivatives Catechin 291.1 139.1 2.99 290.079 [M+H]+ C06562
36 Catechin derivatives Protocatechuic aldehyde 137.1 137 3.06 138.032 [M−H]− C16700
37 Catechin derivatives L-Epicatechin 289 78.8 3.18 290.3 [M−H]− C09727
38 Catechin derivatives Epigallate catechin gallate (EGCG) 459 139.1 3.32 458.085 [M+H]+ C09731
39 Catechin derivatives Catechin–catechin–catechin 865.1 407.2 3.44 866.1 [M−H]− –
40 Catechin derivatives Epicatechin-epiafzelechin 561.1 271.3 3.61 562.1 [M−H]− –
41 Catechin derivatives Epicatechin gallate (ECG) 441.3 289.1 3.89 442.3 [M−H]− –
42 Cholines Choline 104.1 60.2 0.76 103.1 [M+H]+ C00114
43 Cholines O-Phosphocholine 184 83.2 0.78 183 [M+H]+ C00588
44 Cholines sn-Glycero-3-phosphocholine 258.2 125.2 0.78 258.2 [M+H]+ C00670
45 Cholines Acetylcholine 147.1 88 0.85 146.1181 [M+H]+ C08201
46 Coumarins Esculetin (6,7-dihydroxycoumarin) 177 133.1 3.24 178.027 [M−H]− C09263
47 Coumarins Daphnetin 179 179 3.31 178.027 [M+H]+ C03093
48 Coumarins O-Feruloyl 2-hydroxylcoumarin 339.1 177.5 3.32 338.1 [M+H]+ –
49 Coumarins O-Feruloyl 3-hydroxylcoumarin 339.1 177.5 3.34 338.1 [M+H]+ –
50 Coumarins N-sinapoyl hydroxycoumarin 369.1 207.5 3.82 368.1 [M+H]+ –
51 Coumarins O-Feruloyl 4-hydroxylcoumarin 339.1 177.5 3.88 338.1 [M+H]+ –
52 Coumarins Scopoletin (7-Hydroxy-5-methoxycoumarin) 193.1 178.1 4 192.042 [M+H]+ C01752
53 Coumarins Scoparone 207.1 207.1 4.73 206.058 [M+H]+ C09311
54 Coumarins 3,4-Dihydrocoumarin 149.2 107 5.63 148.052 [M+H]+ C02274
55 Coumarins 6-MethylCoumarin 161 105.1 5.96 160.052 [M+H]+ –
56 Flavanone Afzelechin (3,5,7,4′-Tetrahydroxyflavan) 275 139.1 3.4 274.084 [M+H]+ C09320
57 Flavanone Hesperetin 5-O-glucoside 463.1 301.1 3.85 464.132 [M−H]− –
58 Flavanone Hesperetin O-malonylhexoside 549.2 387.3 3.99 550.2 [M−H]− –
59 Flavanone Naringenin 7-O-glucoside (Prunin) 433.1 122.9 4.22 434.1213 [M−H]− C09099
60 Flavanone Naringenin O-malonylhexoside 521 317.6 4.5 520 [M+H]+ –
61 Flavanone Liquiritigenin 255 119 5.16 256.074 [M−H]− C09762
62 Flavanone Butein 271.1 135.1 5.49 272.069 [M−H]− C08578
63 Flavanone Phloretin 273.1 167.1 5.56 274.084 [M−H]− C00774
64 Flavanone Naringenin chalcone 273.1 153.1 5.57 272.069 [M+H]+ C06561
65 Flavanone Naringenin 273.1 153.1 5.59 272.0685 [M+H]+ C00509
66 Flavanone Isoliquiritigenin 255 119.1 6.09 256.074 [M−H]− C08650
67 Flavanone 7-O-Methyleriodictyol 301.1 135.1 6.28 302.079 [M−H]− –
68 Flavanone 4′-Hydroxy-5,7-dimethoxyflavanone 299.1 74.8 6.78 300.1 [M−H]− –
69 Flavanone Isosakuranetin (4′-Methylnaringenin) 287.1 161.1 6.81 286.084 [M+H]+ C05334
70 Flavanone Pinocembrin (Dihydrochrysin) 257.1 153 7.05 256.074 [M+H]+ C09827
71 Flavanone Xanthohumol 355.2 178.9 8.4 354.147 [M+H]+ C16417
72 Flavone Chrysoeriol O-hexosyl-O-malonylhexoside 709.1 547.3 2.49 710.1 [M−H]− –
73 Flavone Acacetin O-acetyl hexoside 487.1 283.2 2.63 488.1 [M−H]− –
74 Flavone Luteolin O-hexosyl-O-hexosyl-O-hexoside 771.1 609.5 2.83 772.1 [M−H]− –
75 Flavone Selgin 5-O-hexoside 479.1 302.8 3.52 478.1 [M+H]+ –
76 Flavone Tricin O-sinapic acid 535 329.4 3.75 536 [M−H]− –
77 Flavone Tricin O-saccharic acid 521.1 329.3 3.81 522.1 [M−H]− –
78 Flavone Luteolin 7-O-glucoside (Cynaroside) 449.1 287.1 3.87 448.101 [M+H]+ C03951
79 Flavone Chrysoeriol O-acetylhexoside 503.1 341.3 3.94 504.1 [M−H]− –
80 Flavone Apigenin 7-O-neohesperidoside (Rhoifolin) 579.2 271.1 4.01 578.1636 [M+H]+ C12627
81 Flavone Apigenin 7-rutinoside (Isorhoifolin) 579.2 271.1 4.01 578.1636 [M+H]+ –
82 Flavone Chrysoeriol O-rhamnosyl-O-glucuronic acid 621.1 299.4 4.07 622.1 [M−H]− –
83 Flavone Tricin di-O-hexoside 655.2 331.7 4.16 654.2 [M+H]+ –
84 Flavone Syringetin 5-O-hexoside 509.2 347.6 4.17 508.2 [M+H]+ –
85 Flavone Syringetin 7-O-hexoside 509.3 283.6 4.17 508.3 [M+H]+ –
86 Flavone Selgin O-hexosyl-O-hexoside 641.1 479.5 4.39 640.1 [M+H]+ –
87 Flavone Spinacetin 347 288 4.41 346 [M+H]+ –
88 Flavone Chrysoeriol O-malonylhexoside 549.1 301.7 4.55 548.1 [M+H]+ –
89 Flavone Tricin O-malonylhexoside 579.1 331.7 4.56 578.1 [M+H]+ –
90 Flavone 7,4′-Dihydroxyflavone 255.1 137.1 4.57 254.058 [M+H]+ C12123
91 Flavone Apigenin 4-O-rhamnoside 417.1 270.9 4.9 416.111 [M+H]+ –
92 Flavone Chrysoeriol O-sinapoylhexoside 669 301.6 4.92 668 [M+H]+ –
93 Flavone Chrysin 5-O-glucoside (Toringin) 417.1 255.7 5 416.1 [M+H]+ –
94 Flavone Luteolin 287.1 287.1 5 286.1 [M+H]+ C01514
95 Flavone Acetyl-eriodictyol O-hexoside 491.1 287.3 5.16 492.1 [M−H]− –
96 Flavone Chrysin O-malonylhexoside 503 255.6 5.24 502 [M+H]+ –
97 Flavone Butin 273.1 153.1 5.59 272.069 [M+H]+ C09614
98 Flavone Apigenin 271.1 215.1 5.63 270.0528 [M+H]+ C01477
99 Flavone Tricin 331.1 315.8 5.74 330.1 [M+H]+ –
100 Flavone Chrysoeriol 301.1 286.1 5.77 300.0634 [M+H]+ C04293
101 Flavone Tricin 7-O-acetylglucoside 535.3 487.2 5.78 534.3 [M+H]+ –
102 Flavone Amentoflavone 539.1 403 5.88 538.09 [M+H]+ C10018
103 Flavone Baicalein (5,6,7-Trihydroxyflavone) 269.1 251.1 5.94 270.053 [M−H]− C10023
104 Flavone Chrysin 255.1 69.7 6.95 254.0579 [M+H]+ C10028
105 Flavone sakuranetin 287.1 287.1 6.96 286.084 [M+H]+ C09833
106 Flavone Acacetin 283.1 268 7.06 284.069 [M−H]− C01470
107 Flavone Nobiletin 403.1 373.1 7.06 402.132 [M+H]+ C10112
108 Flavone Velutin 313.1 298.3 7.22 314.1 [M−H]− –
109 Flavone Tangeretin 373.1 373.1 7.54 372.121 [M+H]+ C10190
110 Flavone C-glycosides 8-C-hexosyl-hesperetin O-hexoside 627.1 430 2.78 626.1 [M+H]+ –
111 Flavone C-glycosides 6-C-hexosyl-luteolin O-hexoside 611.1 329 3.09 610.1 [M+H]+ –
112 Flavone C-glycosides Eriodictiol C-hexosyl-O-hexoside 613.1 300.3 3.09 612.1 [M+H]+ –
113 Flavone C-glycosides C-hexosyl-chrysoeriol O-hexoside 625.2 463.6 3.37 624.2 [M+H]+ –
114 Flavone C-glycosides Eriodictyol C-hexoside 449.1 329.3 3.37 450.1 [M−H]− –
115 Flavone C-glycosides 6-C-hexosyl-hesperetin O-hexoside 627.1 447.3 3.41 626.1 [M+H]+ –
116 Flavone C-glycosides Luteolin 6-C-glucoside 449.1 300 3.45 448.1 [M+H]+ –
117 Flavone C-glycosides Luteolin C-hexoside 449.1 329.6 3.45 448.1 [M+H]+ –
118 Flavone C-glycosides C-hexosyl-luteolin O-hexosyl-O-salicylic acid 731.1 431.5 3.55 730.1 [M+H]+ –
119 Flavone C-glycosides C-hexosyl-apigenin O-pentoside 565.1 397.8 3.6 564.1 [M+H]+ –
120 Flavone C-glycosides di-C,C-hexosyl-apigenin 595.1 415.4 3.68 594.1 [M+H]+ –
121 Flavone C-glycosides Vitexin 2″-O-β-L-rhamnoside 579 433.1 3.68 578.164 [M+H]+ C12628
122 Flavone C-glycosides C-hexosyl-luteolin O-p-coumaroylhexoside 757.2 757 3.73 756.2 [M+H]+ –
123 Flavone C-glycosides 8-C-hexosyl-luteolin O-hexoside 611.1 299.8 3.75 610.1 [M+H]+ –
124 Flavone C-glycosides Apigenin C-glucoside 433.1 271.7 3.78 432.1 [M+H]+ –
125 Flavone C-glycosides Isovitexin 431.1 431.1 3.79 432.1056 [M−H]− C01714
126 Flavone C-glycosides Naringenin C-hexoside 435.1 339.7 3.79 434.1 [M+H]+ –
127 Flavone C-glycosides Acacetin C-hexoside 447.1 298 3.84 446.1 [M+H]+ –
128 Flavone C-glycosides O-methylnaringenin C-pentoside 419.1 383.9 3.84 418.1 [M+H]+ –
129 Flavone C-glycosides C-hexosyl-luteolin O-feruloylpentoside 757.1 739 3.87 756.1 [M+H]+ –
130 Flavone C-glycosides Chrysoeriol 8-C-hexoside 463.1 367.8 3.89 462.1 [M+H]+ –
131 Flavone C-glycosides Chrysin C-hexoside 417.2 381.9 4 416.2 [M+H]+ –
132 Flavone C-glycosides C-pentosyl-apigenin O-p-coumaroylhexoside 711.2 693.1 4.1 710.2 [M+H]+ –
133 Flavone C-glycosides C-pentosyl-chrysoeriol 7-O-feruloylhexoside 771.2 177.5 4.25 770.2 [M+H]+ –
134 Flavone C-glycosides 8-C-hexosyl-apigenin O-feruloylhexoside 771.2 753 4.26 770.2 [M+H]+ –
135 Flavone C-glycosides Apigenin 6-C-pentoside 403.1 367.7 4.3 402.1 [M+H]+ –
136 Flavone C-glycosides Apigenin 8-C-pentoside 403.1 367.6 4.32 402.1 [M+H]+ –
137 Flavonol Quercetin 5-O-malonylhexosyl-hexoside 713.1 713.1 2.96 712.1 [M+H]+ –
138 Flavonol Dihydromyricetin 321.1 153.1 3.52 320.053 [M+H]+ C02906
139 Flavonol Myricetin 3-O-galactoside 479.1 317.3 3.53 480.09 [M−H]− –
140 Flavonol Fustin 289 215.1 3.65 288.063 [M+H]+ C01378
141 Flavonol Quercetin 7-O-rutinoside 611.2 303.7 3.7 610.2 [M+H]+ –
142 Flavonol Kaempferol 3,7-dirhamnoside (Kaempferitrin) 579.2 433.1 3.74 578.164 [M+H]+ C16981
143 Flavonol Kaempferol 3-O-robinobioside (Biorobin) 595.2 287 3.76 594.159 [M+H]+ –
144 Flavonol Quercetin O-acetylhexoside 505.1 301.2 3.8 506.1 [M−H]− –
145 Flavonol Quercetin 4′-O-glucoside (Spiraeoside) 465 302.9 3.86 464.096 [M+H]+ –
146 Flavonol Kaempferol 3-O-galactoside (Trifolin) 449 286.9 3.87 448.101 [M+H]+ C12626
147 Flavonol Quercetin 3-O-glucoside (Isotrifoliin) 465 302.8 3.87 464.096 [M+H]+ C05623
148 Flavonol Quercetin 3-α-L-arabinofuranoside (Avicularin) 435.1 303 3.98 434.0849 [M+H]+ –
149 Flavonol Kaempferide 301.1 259.1 4.13 300.1 [M+H]+ C10098
150 Flavonol Dihydroquercetin (Taxifolin) 303.1 125.1 4.15 304.058 [M−H]− C01617
151 Flavonol Isorhamnetin 5-O-hexoside 479.2 317.8 4.17 478.2 [M+H]+ –
152 Flavonol Kaempferol 3-O-rhamnoside (Kaempferin) 431 285.1 4.48 432.106 [M−H]− C16911
153 Flavonol Aromadedrin (Dihydrokaempferol) 287.1 125.1 4.62 288.063 [M−H]− C00974
154 Flavonol Myricetin 319 319 4.7 318.038 [M+H]+ C10107
155 Flavonol Quercetin-3,4′-O-di-β-glucopyranoside 627.1 465.2 4.83 626.1 [M+H]+ –
156 Flavonol Kaempferol 7-O-rhamnoside 433.1 287 4.94 432.106 [M+H]+ –
157 Flavonol Morin 301 151.1 5.11 302.04265 [M−H]− C10105
158 Flavonol Quercetin 303 303 5.13 302.043 [M+H]+ C00389
159 Flavonol Laricitrin 333 305.2 5.15 332.053 [M+H]+ C12633
160 Flavonol Kaempferol 285 214 5.73 286.048 [M−H]− C05903
161 Flavonol Syringetin 347 287.1 5.8 346.069 [M+H]+ C11620
162 Flavonol Isorhamnetin 315.1 300.1 5.85 316.058 [M−H]− C10084
163 Flavonol Di-O-methylquercetin 329.1 314.3 5.91 330.1 [M−H]− –
164 Flavonol Ayanin 345.2 177.5 6.33 344.2 [M+H]+ C04444
165 Flavonol Rhamnetin (7-O-methxyl quercetin) 317 317 6.43 316.058 [M+H]+ C10176
166 Flavonol 3,7-Di-O-methylquercetin 329 314 6.63 330.074 [M−H]− C01265
167 Flavonol Troxerutin (Trihydroxyethyl rutin) 347.3 285.4 6.66 346.251 [M+H]+ –
168 Flavonol Kumatakenin 315.1 300 7.23 314.079 [M+H]+ –
169 Flavonolignan Tricin 4′-O-(syringyl glyceryl)ether 557.2 331.9 4.44 556.2 [M+H]+ –
170 Flavonolignan Tricin 7-O-β-guaiacylglycerol 527.1 331.7 5.44 526.1 [M+H]+ –
171 Flavonolignan Tricin 4′-O-syringyl alcohol 497.1 331.8 5.75 496.1 [M+H]+ –
172 Flavonolignan Tricin 4′-O-β-guaiacylglycerol 527.1 331.7 5.84 526.1 [M+H]+ –
173 Hydroxycinnamoyl derivatives Caftaric acid 311.1 149.2 2.16 312.1 [M−H]− –
174 Hydroxycinnamoyl derivatives O-Caffeoyl maltotriose 665.1 323.4 2.23 666.1 [M+H]+ –
175 Hydroxycinnamoyl derivatives Syringin 371.1 209.2 2.58 372.142 [M+H]+ C01533
176 Hydroxycinnamoyl derivatives Coniferin 341 179.1 2.72 342.132 [M−H]− C00761
177 Hydroxycinnamoyl derivatives Caffeic acid O-glucoside 341 179.2 2.86 342 [M−H]− –
178 Hydroxycinnamoyl derivatives Homovanillic acid 181.1 137.1 3.04 182.0579 [M+H]+ C05582
179 Hydroxycinnamoyl derivatives Hydroxy-methoxycinnamate 195.1 177.5 3.22 194.1 [M+H]+ –
180 Hydroxycinnamoyl derivatives 1-O-β-d-Glucopyranosyl sinapate 385.1 223.2 3.26 386.1 [M−H]− –
181 Hydroxycinnamoyl derivatives 6-Hydroxymethylherniarin 207.1 147.4 3.31 206.1 [M+H]+ –
182 Hydroxycinnamoyl derivatives Vanillic acid 169 111 3.35 168.042 [M+H]+ C06672
183 Hydroxycinnamoyl derivatives Syringic acid 197.1 122.9 3.38 198.0528 [M−H]− C10833
184 Hydroxycinnamoyl derivatives Feruloyl syringic acid 375.2 137.6 3.47 374.2 [M−H]− –
185 Hydroxycinnamoyl derivatives p-Coumaryl alcohol 149 130.1 3.67 150.068 [M−H]− C02646
186 Hydroxycinnamoyl derivatives 3-(4-Hydroxyphenyl)propionic acid 165.1 92.9 3.84 166.063 [M−H]− C01744
187 Hydroxycinnamoyl derivatives p-Coumaric acid 163 119 3.86 164.047 [M−H]− C00811
188 Hydroxycinnamoyl derivatives Coniferyl alcohol 179.1 146.1 3.88 180.079 [M−H]− C00590
189 Hydroxycinnamoyl derivatives Sinapyl alcohol 209 179.1 3.88 210.089 [M+H]+ C02325
190 Hydroxycinnamoyl derivatives Ferulic acid 193.1 134.1 4.07 194.0579 [M+H]+ C01494
191 Hydroxycinnamoyl derivatives 3-Hydroxy-4-methoxycinnamic acid 193.1 134.1 4.08 194.0579 [M−H]− –
192 Hydroxycinnamoyl derivatives 2-Methoxybenzoic acid 151 136.1 4.16 152.0473 [M−H]− –
193 Hydroxycinnamoyl derivatives p-Coumaraldehyde 149.1 131 4.42 148 [M−H]− –
194 Hydroxycinnamoyl derivatives Resveratrol 229.1 135 4.59 228.079 [M−H]− C03582
195 Hydroxycinnamoyl derivatives Sinapinaldehyde 207.1 177.1 4.61 208 [M−H]− –
196 Hydroxycinnamoyl derivatives Coniferylaldehyde 179.1 123 4.64 178.063 [M−H]− C02666
197 Hydroxycinnamoyl derivatives Pinoresinol 357.1 136.1 5.41 358.142 [M+H]+ –
198 Hydroxycinnamoyl derivatives 4-Methoxycinnamic acid 177 145.2 5.5 178 [M−H]− –
199 Hydroxycinnamoyl derivatives 3,4-Dimethoxycinnamic acid 207.1 192.1 5.52 208.1 [M−H]− –
200 Hydroxycinnamoyl derivatives trans-cinnamaldehyde 133.1 115 5.97 132.0575 [M+H]+ C00903
201 Hydroxycinnamoyl derivatives Caffeic aldehyde 165.1 95.5 6.04 164.1 [M+H]+ C10945
202 Hydroxycinnamoyl derivatives Syringaldehyde 183.1 165.5 6.58 182.1 [M−H]− –
203 Hydroxycinnamoyl derivatives Methyleugenol 179 138 7.3 178.099 [M−H]− C10454
204 Hydroxycinnamoyl derivatives Caffeyl alcohol 317.2 281.3 7.47 316 [M+H]+ C09066
205 Isoflavone Daidzein 7-O-glucoside (Daidzin) 417.1 255.1 3.36 416.111 [M+H]+ C10216
206 Isoflavone Glycitin 445 282.1 3.54 446.121 [M+H]+ C16195
207 Isoflavone Genistein 7-O-Glucoside (Genistin) 433 270.9 4.01 432.106 [M−H]− C09126
208 Isoflavone Formononetin 7-O-glucoside (Ononin) 429.1 267.1 4.59 430.126 [M+H]+ C10509
209 Isoflavone 2′-Hydroxygenistein 287 217.1 4.89 286.048 [M−H]− C12134
210 Isoflavone Daidzein 255.1 199.1 4.89 254.0579 [M+H]+ C10208
211 Isoflavone Orobol (5,7,3′,4′-tetrahydroxyisoflavone) 285 257.1 5.08 286.048 [M−H]− C10510
212 Isoflavone Sissotrin 447.1 285.1 5.16 446.121 [M−H]− C05376
213 Isoflavone Formononetin (4′-O-methyldaidzein) 269.1 269.1 6.33 268.074 [M+H]+ C00858
214 Isoflavone Prunetin 283 268.1 6.97 284.069 [M−H]− C10521
215 Phenolamides Spermidine 146.2 72.1 0.56 145.2 [M+H]+ C00315
216 Phenolamides Spermine 203 112 0.62 202 [M+H]+ C00750
217 Phenolamides Putrescine 89 71.9 0.64 88.1 [M+H]+ C00134
218 Phenolamides Agmatine 131.1 72.1 0.75 130.1 [M+H]+ C00179
219 Phenolamides 1,5-Diaminopentane 103 86.1 0.76 102.116 [M+H]+ C01672
220 Phenolamides N-Acetylputrescine 131 71.9 0.8 130.11061 [M+H]+ C02714
221 Phenolamides N-hexosyl-p-coumaroyl putrescine 397.1 147.4 1.73 396.1 [M+H]+ –
222 Phenolamides N-Caffeoyl putrescine 251.1 233.5 1.97 250.1 [M+H]+ C03002
223 Phenolamides N-(4′-O-glycosyl)-p-coumaroyl agmatine 439.1 147.4 2.11 438.1 [M+H]+ –
224 Phenolamides N′,N″,N″′-p-coumaroyl-cinnamoyl-caffeoyl spermidine 584.2 325.8 2.42 583.2 [M+H]+ –
225 Phenolamides N′, N″-di-p-coumaroylspermine 495.3 478.4 2.43 494.3 [M+H]+ –
226 Phenolamides N′-Feruloyl putrescine 265.1 177.5 2.44 264.1 [M+H]+ –
227 Phenolamides N-Caffeoyl agmatine 293.2 234.5 2.45 292.2 [M+H]+ –
228 Phenolamides N-Sinapoyl putrescine 295 207.6 2.77 294 [M+H]+ –
229 Phenolamides N′, N″-disinapoylspermidine 558.3 264.8 3.75 557.3 [M+H]+ –
230 Proanthocyanidins Procyanidin B3 577.1 407.3 2.79 578.1424 [M−H]− –
231 Proanthocyanidins Procyanidin A3 577.1 425.4 2.92 576.1 [M+H]+ –
232 Proanthocyanidins Procyanidin B2 579.1 127.3 3.03 578.1424 [M+H]+ –
233 Proanthocyanidins Procyanidin A1 575 285.3 3.68 576.1268 [M−H]− –
234 Proanthocyanidins Procyanidin A2 577 425.9 4.06 576.1268 [M+H]+ C10237
235 Quinate and its derivatives Quinic acid 191 85 0.92 192.063 [M−H]− C00296
236 Quinate and its derivatives p-Coumaroyl quinic acid O-glucuronic acid 513.1 191.2 1.82 514.1 [M−H]− –
237 Quinate and its derivatives Quinacyl syringic acid 371.1 179.2 1.85 372.1 [M−H]− –
238 Quinate and its derivatives Homovanilloyl quinic acid 355.1 181.2 1.89 356.1 [M−H]− –
239 Quinate and its derivatives 5-O-p-coumaroyl quinic acid O-hexoside 499.1 163.2 2.1 500.1 [M−H]− –
240 Quinate and its derivatives O-Feruloyl quinic acid 369.1 177.5 2.12 368.1 [M+H]+ –
241 Quinate and its derivatives Quinic acid O-di-glucuronic acid 543.1 191.2 2.13 544.1 [M−H]− –
242 Quinate and its derivatives Neochlorogenic acid (5-O-Caffeoylquinic acid) 353 191.1 2.35 354.095 [M−H]− C17147
243 Quinate and its derivatives 1-O-Caffeoyl quinic acid 353.1 191.1 2.38 354.095 [M−H]− –
244 Quinate and its derivatives 3-O-p-coumaroyl quinic acid O-hexoside 499.2 173.2 2.45 500.2 [M−H]− –
245 Quinate and its derivatives 5-O-p-coumaroyl shikimic acid O-hexoside 481.1 445.4 2.62 482.1 [M−H]− –
246 Quinate and its derivatives Chlorogenic acid (3-O-Caffeoylquinic acid) 353.1 191.1 2.72 354.0951 [M−H]− C00852
247 Quinate and its derivatives 1-O-p-Coumaroyl quinic acid 337.1 155.8 2.85 338.1 [M−H]− –
248 Quinate and its derivatives 4-O-Caffeoyl quinic acid (criptochlorogenic acid) 353.1 191.2 3 354.1 [M−H]− –
249 Quinate and its derivatives 3-O-Feruloyl quinic acid 369.1 177.5 3.01 368.1 [M+H]+ C02572
250 Quinate and its derivatives O-Sinapoyl quinic acid 399 207.5 3.17 398 [M+H]+ –
251 Quinate and its derivatives 3-O-p-coumaroyl shikimic acid O-hexoside 481.1 319.3 3.23 482.1 [M−H]− –
252 Quinate and its derivatives 5-O-p-Coumaroylquinic acid 337 275.8 3.26 338 [M−H]− –
253 Quinate and its derivatives 3-O-p-Coumaroyl quinic acid 337.1 190.9 3.3 338.1 [M−H]− –
254 Quinate and its derivatives 1-O-Feruloyl quinic acid 369.1 207.5 3.42 368.1 [M+H]+ –
255 Quinate and its derivatives Chlorogenic acid methyl ester 367 179.1 3.64 368.111 [M−H]− –
256 Quinate and its derivatives 5-O-p-Coumaroyl shikimic acid 321.1 147.5 3.81 320.1 [M+H]+ –
257 Quinate and its derivatives 3-O-p-Coumaroyl shikimic acid 319 145.3 3.93 320 [M−H]− –
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Absolute quantification of catechin derivatives and total proanthocyanidins (PAs) contents

Current study reports developmental stage dependent variation (Fig. 3A) in total proanthocyanidins (PAs) contents using a method described by Dong et al.34. Pulp samples of both cultivars contain similar quantities of PAs. However, there is an increasing trend for PAs contents towards fruit maturity in both cultivars (Fig. 3B). Fruit peels of both cultivars contain higher amount of PAs as compared to pulps. For TN cultivar, the concentration of peel PAs remained in close range across three growth stages. However, there was a massive increase in PAs content of HGF cultivar towards maturity (Fig. 3B). Very few studies have documented the concentration of PAs in mango and it is often influenced by several factors including tissue type, geographical area and method of extraction33,35–37. Pulp of mangoes from USA were reported to contain 12.8 mg proanthocyanidins/100 g fresh weight. Two different extraction methods yielded 0.18 and 0.48 mg PAs per 100 g DW of mangoes from Spain36. Similarly, procyanidins A2 (14–78 µg /ml), B1 (29–88 µg /ml) and B2 (0–10 µg /ml) were reported in peel liqueurs of mangoes from Brazil37.

Figure 3.

Figure 3

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Fruit color and total proanthocyanidin (PA) contents of Hongguifei (HGF) and Tainong (TN) mango.

The phenolic compounds are among the major contributors that are accountable for antioxidant properties in fruits, vegetables, whole grains and other plant-based materials38. The TN mango fruit contains higher levels of total phenolics (TPs) and total flavonoids as compared to HGF2. However, total anthocyanin contents (TAs) were reported to be higher in HGF as compared to TN2. In phenylpropanoid biosynthesis pathway, both anthocyanins and proanthocyanins belong to the terminal steps39. Therefore, the increase in PAs (Fig. 3) potentially correlates with anthocyanins2 in HGF mango.

In order to validate the results of metabolome based estimation of relative quantities of catechin and derivatives, absolute quantities of catechin and its derivatives were calculated in peel and pulp samples of both cultivars using HPLC. It was observed that the concentrations of catechin, gallocatechin, gallocatechin gallate, epicatechin, epicatechin gallate, epicatechin-3-O-gallate, protocatechuic aldehyde, 3,4-Dihydroxybenzoic acid and ellagic acid were differentially present in both cultivars for pulp and peel samples (Fig. 4). Overall, peel samples contained higher amounts of these metabolites that decreased with the age of fruit40. Moreover, fold change modifications of these metabolites follow similar trend (with minor variations) as discussed above (Table S2). In previous studies, these compounds were either individually reported as catechine41, epicatechin42, protocatechuic acid2 and ellagic acid or in terms of total proanthocyanidin and tannins10. The composition of phenolic compounds in peels has attracted a crucial importance for mango in calculating functional food mixtures43.

Figure 4.

Figure 4

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HPLC based quantification of Catechin, derivatives and phenolic acids in the pulp and peel of both cultivars. TNS and HGFS represent quantification in peel of respective cultivars. TN and HGF represent quantification in pulp of respective cultivars. The letters D, E and R represent development, enlargement and ripening of mango fruit. The use of commercial standards for the quantification of catechin derivatives and phenolic acids along with linear equations, correlation coefficients, LOD’s, and LOQ’s values are presented in Table S5.

Differential expression of MiANR and MiLAR genes

The genes encoding anthocyanidin reductase (ANR) and leucoanthocyanidin reductase (LAR) enzyme have been cloned and characterized in plants including poplar, buckwheat, lotus and fruits such as grapevine, strawberry, persimmon, apple, and mango (for references see44). The expression patterns of these genes are highly correlated with PA accumulation in many plants. To determine whether the differential expression of catechin/derivatives correlated with the transcript abundance of MiANR and MiLAR, the expression levels of these genes were analyzed in fruits of both cultivars using relative qRT-PCR (Fig. 5). In pulp samples, both genes exhibited an opposite expression profile i.e., the expression of MiANR increased with fruit maturity in HGF and MiLAR followed similar pattern in TN cultivar. In peel samples of both cultivars, the relative difference of expression increased (with fruit maturity) for MiANR and decreased (with fruit maturity) for MiLAR (Fig. 5). These results suggested that transcription of LAR and ANR seems controlled by a feedback mechanism45. It means a higher concentration of catechin may stimulate the expression of LAR and higher levels of epicatechin can promote the expression of anthocyanidin synthase (ANS) and ANR. In addition, there could be a potential competition between LAR and ANR enzymes. The activity of both of these reductases (ANR and LAR) is dependent on NAPDH. Therefore, if one of them is overexpressed, it will decrease the availability of NAPDH for the other enzyme. It is expected that such competition may govern the mutual inhibition of LAR and ANR expression observed in this study. Altogether, the PA biosynthesis is likely co-regulated by structural genes such as LAR and ANR, and the mutual inhibition between the ANR and LAR expression may affect PA accumulation16. A lack of clear association between the transcripts of LAR/ANR and the catechin/derivatives has already been reported in other plants as well40,46. Earlier studies indicate a potential importance of ANR and LAR genes in the biosynthesis of galloylated catechins47. Therefore, it could be explained in terms of variable amounts of catechin/derivatives and the fact that different forms of catechin are potentially interconvertible.

Figure 5.

Figure 5

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Relative RT-qPCR analysis of MiANR and MiLAR gene.

In each comparison, the default expression value of both genes was adjusted to one in samples obtained from TN cultivar.

Materials and methods

Plant material, sample preparation and extraction

Current study compares metabolites of fruit peel and pulp of two mango varieties named Tainong (TN) and Hongguifei (HGF), during three different developmental stages of fruit (Development or 1st, Enlargement or 2nd, and Ripening or 3rd). Both varieties were maintained at a farm located at Basuo town, Dongfang County, Hainan province. The TN mango was developed by the Fengshan tropical horticulture branch institute of the Taiwan Agricultural Test Institute and introduced to southern provinces of China including Hainan and Guangdong in 1994. The TN fruit is oval-shaped and relatively small in size that weighs up to 300 g. Mature fruit peel is dark green to greenish-yellow. The peel is slightly thicker and ductile, which is good for storage and transportation The HGF mango, also known as Hongjinglong, is native to Taiwan. It is a hybrid of 'Irwin' and 'Kate' and was introduced to Hainan in the 1990s48,49. The HGF mango fruit is oblong, the top of the fruit is small and the fruit is relatively large (300–500 g). Mature fruit peel is purple-red and green (Fig. 3A).

Fruit samples from both varieties were collected at 40 (Developmental or 1st), 65 (Enlargement or 2nd), and 90 (Ripening or 3rd) days after full bloom (DAFB) respectively. Samples for each stage consisted of 10 fruits from 10 mango trees. Fruits of each variety were peeled and cored, and the flesh was cut into small sections. Fruit samples at each stage were mixed and immediately frozen in liquid nitrogen, and then stored at − 80 °C until used.

A mixer mill with zirconia bead (MM 400, RETSCH) was used to grind the freeze-dried samples for 90 s at 30 Hz. Then, an overnight extraction (at 4 °C using 70% aqueous methanol) was performed for 100 mg powder. Before LC–MS analysis, the samples were centrifuged at 10,000×g for 10 min followed by filtration (SCAA-104, 0.22 μm pore size; ANPEL, Shanghai, China, https://www.anpel.com.cn/).

HPLC analysis

An LC–ESI–MS/MS system (HPLC, Shim-pack UFLC SHIMADZU CBM30A system, www.shimadzu.com.cn/; MS, Applied Biosystems4500 Q TRAP, www.appliedbiosystems.com.cn/) was used to analyze the sample extracts. The analytical parameters were as follow: HPLC column, waters ACQUITY UPLC HSS T3 C18 (1.8 µm, 2.1 mm * 100 mm); solvent system, water (0.04% acetic acid): acetonitrile (0.04% acetic acid); gradient program, 100:0 V/V at 0 min, 5:95 V/V at 11.0 min, 5:95 V/V at 12.0 min, 95:5 V/V at 12.1 min, 95:5 V/V at 15.0 min; flow rate, 0.40 mL/min; temperature, 40 °C; injection volume: 5 μl. The effluent was alternatively connected to an ESI-triple quadrupole-linear ion trap (Q TRAP)-MS.

ESI-Q TRAP-MS/MS

Triple quadrupole-linear ion trap mass spectrometer (QTRAP; API 4500 Q TRAP LC/MS/MS System) was used for Linear Ion Trap (LIT) and triple quadrupole (QQQ) scans. The equipment contained an ESI Turbo Ion-Spray interface, which was operated in a positive and negative ion-mode and the data was analyzed using analyst 1.6 software (AB SCIEX). The chromatographic method (e.g., mobile phase composition, pH, elution gradient) is the same in both ESI acquisition modes. Following conditions were used for the source of ESI operation: turbo spray (ion-source); 550 °C (source temperature); 5500 V (ion spray voltage or IS); GSI (ion source gas I), GSII (gas II), CUR (curtain gas) were set at 55, 60, and 25.0 psi, respectively; CAD (the collision gas) was set at high. Polypropylene glycol (10 and 100 μmol/L) was used to tune the instrument and for calibration of mass in QQQ and LIT modes, respectively. The collision gas (N2) was set to 5 psi during QQQ scans based MRM analysis. A specific set of MRM transitions were monitored for each period according to the metabolites eluted within this period.

Quantitative and qualitative principles of metabolites

Based on the public database and the self-built database MWDB (metware) of metabolite information, the first-order spectrum and two-level spectral data of spectral detection were qualitatively analyzed. The structural analysis of metabolites is referenced by knapsack (https://kanaya.naist.jp/KNApSAcK/), Massbank (https://www.massbank.jp/), Metlin (https://metlin.scripps.edu/index.php), MoTo DB (https://www.ab.wur.nl/moto/), hmdb (https://www.hmdb.ca/), and other existing mass spectrometry public databases. The quantification of metabolites was accomplished using the multi-reaction monitoring model of the triple four-stage rod mass spectrometry (multiple reaction monitoring, MRM). The detection standard of MRM is based on the parameters including Q1, Q3, RT, DP, CE from the database, which was built using the standards. The relative content of the compounds was determined by the signal intensity of Characteristic fragment ion Q3. The range of DP (declustering potential) was − 80 to 80 V and CE (collision energy) was − 50 to 50 V. In MRM mode, the four levers first filter the precursor ions of the target, the ions matching substances with different molecular weights are excluded for initial removal of disturbance, and the precursor ions are induced by the collision chamber to form many fragments of ions. The fragment ions are then filtered through the triple four-pole filter to select characteristic fragment ions, eliminate non-target ion interference, make the quantification more accurate, and improve repeatability. After obtaining the data of the different samples of the metabolite spectra, the peak area integral of all the material mass spectra was obtained, and the mass spectra of the same metabolites in different samples were corrected by integral correction.

Statistical analysis

The SIMCA14.1 software package (V14.1, Sartorius Stedim Data Analytics AB, Umea, Sweden) was used for principal component analysis (PCA) and orthogonal projections to latent structures-discriminate analysis (OPLS-DA). PCA showed the distribution of the original data. In order to obtain a higher level of group separation and to get a better understanding of variables responsible for classification, supervised OPLS-DA were applied. Based on OPLS-DA, a loading plot was constructed, which showed the contribution of variables to differentiate between two groups. The first principal component of variable importance in the projection (VIP) was calculated to refine this analysis. The VIP values above one were designated as differential metabolites. In the second step, Student’s t-test was used to assess the remaining variables and variables with p value > 0.05 were discarded between two comparison groups. In addition, commercial databases including KEGG50 https://www.genome.jp/kegg/ and MetaboAnalyst https://www.metaboanalyst.ca/ were used to search for the pathways of metabolites.

Determination of total proanthocyanidins (PAs) content

The proanthocaynidins content of the extracts were determined using the method described by DongRuixia[12]. Calibration curve was prepared by mixing methanol solution of standard proanthocyanidin (1 mL; 0.2–1 mg/mL) with 6 mL of 4% (g/v) vanillic aldehyde and 3 mL of concentrated HCl. After capping and shaking the tube, it was incubated in the dark for 15 m at 30℃ ± 1. The absorbance was measured at 500 nm (UVmini-1240, Shimadzu Corporation, Kyoto, Japan) with methanol as blank control and the standard curve was plotted. 1 mL of each of the extract solution in methanol (0.1 g mL−1) was also mixed with the above mentioned reagents, After incubation for 30 min, the absorbance was measured to determine proanthocyanidins content. The concentration of proanthocyanidin of samples was calculated using the following equation based on a PAs standard curve: y = 1.038x + 0.046 Where X is the absorbance and y is the proanthocyanidin equivalent. For the precentage of PAs content in tested samples, the equation is as follow: D = (v Cn/1000 W) 100%. All tests were conducted in triplicate D: the percentage of PAs content of samples; V: The constant volumn of sample; C: the concentration of proanthocyanidin of samples (mg/mL); n: dilution times; W: weight of sample(dry weight). Then the percentage of PAs conent of samples was converted to mg/ 100 g FW based on the ratio of fresh and dry weight of mango.

RNA extraction and relative RT-qPCR analysis

Peel and pulp samples were used for RNA extraction with the help of RNAprep Pur Plant Kit for polysaccharides and polyphenolics-rich samples (TIANGEN Biotech, Beijing) following the instructions of the manufacturer. The concentration of RNA was estimated from each sample through NanoDrop spectrophotometer (BERTHOLD, Germany). All-in-one First-Strand Synthesis Mastermix, with DNaseI (NOVA BIOMED, China) was used to reverse transcribe 1.0 μg of total RNA. The qRT-PCR analysis was performed using an APPLIED BIOSYSTEMS StepOnePlus Real-Time PCR System and TB GREEN Premix Ex Taq II, Tli RNaseH plus kit (TAKARA). The Oligo Calculator (https://mcb.berkeley.edu/labs/krantz/tools/oligocalc.html) was used for designing the gene-specific primers and NCBI Primer-BLAST program (https://www.ncbi.nlm.nih.gov/tools/primer-blast/) was used to verify primer specificity. The expression data were normalized using MiActin gene (GenBank accession number HQ830244) as an internal control. Following primers were used for RT-qPCR: MiANR (Fow-TCCAAGACCCTGGCTGAAAG; Rev-CTGGCGTAAGAGAAGGACCA), MiLAR (Fow-ATTAAACCAGCTCCCTCTCG; Rev-CACATCATGCCCAAACTCAG), and MiActin (Fow-GCTTGCCTATGTTGCCCTTGACTA; Rev-GCATCGGAATCTCTCAGCTCCAAT). An equal amount of cDNA template was used for each sample including the internal control. The qPCR analysis was repeated in three independent experiments.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Conclusions

The current study provides a global picture of metabolite dynamics between two mango cultivars by conducting an analysis of widely-targeted metabolomics based on LC–MS/MS data. The differential accumulation or absence of particular metabolites from either of cultivars indicates underlying differential metabolism. Important metabolites including catechin, its derivatives and procyanidins only up-regulated in HGF pulp and peel samples. The current study revealed that the expression of MiANR (a key gene of the PP pathway) was significantly higher in both pulp and peel samples of HGF cultivar at all three stages of fruit development. Moreover, total proanthocyanidin contents and relative flavan-3-ols/procyanidins were also higher in HGF cultivar. It seems obvious that such variations are directly responsible for the detected differences in relative quantities of flavonoid. This study documented changes in absolute contents of important catechin/ derivatives and expression profile of key genes involved in their biosynthesis for three growth stages. Such knowledge of mango fruit will be helpful for producers in adding value to the fruit and increasing antioxidant components. Moreover, different derivatives show distinct contents towards maturity and higher concentrations in peels as compared to pulp. It advocates the need for further research to improve contents of these metabolites in edible portion of mango.

Supplementary information

Supplementary Figure 1. (630.7KB, tif)
Supplementary Figure 2A. (833.2KB, tif)
Supplementary Figure 2B. (932.1KB, tif)
Supplementary Table 1. (68.2KB, xlsx)
Supplementary Table 2. (358.2KB, xlsx)
Supplementary Table 3. (10.8KB, xlsx)
Supplementary Table 4. (54.7KB, xlsx)
Supplementary Table 5. (9.8KB, xlsx)
Supplementary Legends. (13.7KB, docx)

Acknowledgements

The authors acknowledge the China Science and Technology Exchange Center (CSTEC) for the postdoc fellowship of Farrukh Azeem through Talented Young Scientist Program (TYSP).

Author contributions

Conceptualization, L.T. and F.A.; methodology, F.A. and L.T.; software, C.Z.; validation, F.A., H.N. and G.Y.; formal analysis, F.A. and J.Z.; resources, L.T.; data curation, F.A.; writing—original draft preparation, F.A. and L.T.; writing—review and editing, H.N. and R.Z.; supervision, L.T.; project administration, L.T. and R.Z.; funding acquisition, L.T.

Funding

This research was supported by central public-interest scientific institution basal research fund for the Chinese Academy of Tropical Agricultural Sciences (project no.1630092019006 and 630092018007), and the earmarked fund for the Belt and Road Tropical Project (BARTP-07).

Competing interests

The authors declare no competing interests.

Footnotes

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Farrukh Azeem, Email: azeuaf@hotmail.com.

Rulin Zhan, Email: zhanrulin555@163.com.

Supplementary information

is available for this paper at 10.1038/s41598-020-75636-y.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary Figure 1. (630.7KB, tif)
Supplementary Figure 2A. (833.2KB, tif)
Supplementary Figure 2B. (932.1KB, tif)
Supplementary Table 1. (68.2KB, xlsx)
Supplementary Table 2. (358.2KB, xlsx)
Supplementary Table 3. (10.8KB, xlsx)
Supplementary Table 4. (54.7KB, xlsx)
Supplementary Table 5. (9.8KB, xlsx)
Supplementary Legends. (13.7KB, docx)

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