Current Situation and Perspectives of Fruit Annonaceae in Mexico: Biological and Agronomic Importance and Bioactive Properties
Abstract
:1. Introduction
2. Agronomic Knowledge
2.1. Nutritional Composition
2.2. Tradicional Medicine Use
2.3. Bioactive Compounds Identified in Fruit Annona Species
2.3.1. Phenolic Compounds and Fatty Acids
2.3.2. Cyclopeptides
2.3.3. Alkaloids
2.3.4. Acetogenins (ACGs)
2.4. Biological Activities from Extracts or Isolated Compounds from Annona Species
2.4.1. Cytotoxic Activity
2.4.2. Anti-Hyperglycemic Activity
2.4.3. Anti-Inflammatory
2.5. Technologies for Postharvest Handling
3. Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Parameter | A. muricata | A. cherimola | A. squamosa | A. macroprophyllata |
---|---|---|---|---|
Total Energy (kcal) | 55.4–81.73 | 81–102 | 92.9–97.7 | 56.06–89.03 |
Moisture (%) | 80.48–83.2 | 68.7–70.4 | 65–75 | 71.5–79.61 |
Protein (%) | 0.69–1.10 | 1.36–1.96 | 0.7–1.89 | 0.44–1.31 |
Lipids (%) | 0.20–0.97 | 0.10–0.29 | 0.048–0.57 | 0.16–0.31 |
Soluble carbohydrates (%) | 12.50–18.23 | 13.0–29.0 | 20.41–25.19 | 13.55–20.25 |
Dietary fiber (%) | 4.83–5.76 | 2.09–5.32 | 0.62–1.41 | 0.97–1.30 |
Minerals (mg/100 g) | ||||
Calcium | 9.0–10.3 | 9.0–27.14 | 17.0–44.7 | 0.86–31.60 |
Phosphorous | 27.7–29.0 | 24.0–35.20 | 54.0 | 51.7 |
Iron | 0.64–0.82 | 0.25–0.60 | 0.3–1.34 | ND |
Magnesium | 22.0 | 17 | 21.0–22.0 | 8.0–14.01 |
Copper | ND | ND | 0.086 | ND |
Manganese | ND | ND | 0.10 | ND |
Zinc | ND | 0.16 | 0.1 | 0.10–0.13 |
Potassium | 320 | 288 | 142 | 335.95–347.40 |
Vitamins (mg/100 g) | ||||
Vitamin C | 22.59–40.56 | 12–6–25.43 | 25.6–58.75 | 1.51–13.6 |
Vitamin E | 29 | 0.27 | ND | ND |
Thiamin | 0.11–2.10 | 0.09–0–0.11 | 0.10 | 0.24 |
Riboflavin | 0.05–0.2 | 0.11–0.13 | 0.06 | 0.30 |
Niacin | 0.21–1.52 | 0.65–1.0 | 0.89 | 2.18 |
Cobalamin | ND | 0.12 | ND | ND |
Refences | [70,71] | [72,73,74] | [75,76,77,78] | [76,79] |
Annona Specie | Plant Part | Bioactive Compounds | Content | References |
---|---|---|---|---|
Phenolic compounds | ||||
A. muricata | Pulp (μg/g dw) | Chlorogenic acid | 12.80 | [83] |
Cinnamic acid | 42.04 | |||
Coumaric acid | 0.07 | |||
Gallic acid | 15.86 | |||
4-Hydroxybenzoic acid | 131.63 | |||
Neochlorogenic acid | 72.32 | |||
Dicaffeoylquinic acid, caffeoylquinic acid, fisetin, dihydrokaempferol-hexoside, morin, kaempferol 3-O-rutinoside, kaempferol, luteolin 3′7-di-O-glucoside, myricetin | NR | [90,91,92] | ||
Leaf (μg/g dw) | Caffeoylquinic acid, chlorogenic acid, dicaffeoylquinic acid, feruloylquinic acid, cinnamic acid, isoferulic acid, caffeic acid, gallic acid, apigenin-6-C-glucoside, argentinine, catechin, coumaric acid, daidzein, epicatechin, gallocatechin, genistein, glycitein, homoorientin, kaempferol, kaempferol 3-O-rutinoside, luteolin 3′7-di-O-glucoside, quercetin, quercetin 3-O-glucoside, quercetin 3-O- neohesperidoside, quercetin 3-O-robinoside, quercetin–O-rutinoside, quercetin 3-O-α-rhamnosyl, robinetin, tangeretin, taxifolin (+),vitexin | NR | [90,91,92,98] | |
Peel (μg/g dw) | Gallic acid | 14.50 | [83] | |
Coumaric acid | 1.37 | |||
Cinnamic acid | 45.51 | |||
Caffeic acid | 43.68 | |||
Chlorogenic acid | 32.67 | |||
Protocatechuic acid | 150.46 | |||
4-Hydroxybenzoic acid | 145.98 | |||
Syringic acid | 883.71 | |||
Neochlorogenic acid | 78.86 | |||
Seed (μg/g dw) | Gallic acid | 0.36 | [83] | |
Coumaric acid | 0.07 | |||
Cinnamic acid | 40.48 | |||
Caffeic acid | 32.62 | |||
Chlorogenic acid | 12.33 | |||
Protocatechuic acid | 133.47 | |||
Syringic acid | 780.77 | |||
Neochlorogenic acid | 69.70 | |||
A. cherimola | Pulp | Catechin, procyanidin (B-type) dimer isomer, (epi)catechin-(epi)gallocatechin, epicatechin, derivates of procyanidin trimer | NR | [93] |
Leaf (mg/100 g dw) | Catequin | 12.42–24.5 | [84] | |
Quercetin 3-O-rutinoside-7-O-glucoside | 1.06–16.16 | |||
Epicatechin | 6.33–26.31 | |||
Quercetin 3-O-rutinoside-7-O-pentoside | 32.25–75.29 | |||
Quercetin 3-O-rutinoside | 719.53–2593.92 | |||
Kaempferol-3-Galactoside-7-Rhamnoside | 55.74–620.98 | |||
Kaempferol-3-O-glucoside | 22.44–337.09 | |||
Luteolin-3-Galactoside-7-Rhamnoside | 47.49–120.58 | |||
A. squamosa | Leaf | Quercetin, quercetin 3-O-glucoside, rutin, gallic acid, chlorogenic acid, isorhamnetin, ferulic acid, kaempferol, caffeic acid | NR | [85,95] |
Seed | Gallic acid, ρ-hydroxybenzoic acid, syringic acid, ferulic acid, ellagic acid, benzoic acid, o-coumaric acid, and salicylic acid | NR | [96] | |
A. diversifolia | Peel (mg/100 g) | Chlorogenic acid | 84 | [86] |
Ferulic acid | 34.9 | |||
p-hydroxybenzoic | 20.90 | |||
Caffeic acid | 6.6 | |||
Gallic acid | 4.9 | |||
Epicatechin | 102 | |||
Seed (%) | Oleic acid Palmitic acid Linoleic acid Stearic acid | 70.42 16.40 7.97 5.22 | [79] | |
Palmitic acid | ||||
A. muricata | Seed (%) | Linoleic acid | 25.5 | [97] |
Stearic acid | 1.5 | |||
Stearic acid | 6.0 | |||
Oleic acid | 39.5 | |||
Linoleic acid | 27.0 | |||
A. cherimola | Seed (%) | Myristic acid | 0.05 | [99,100] |
Palmitic acid | 14.91 | |||
Heptadecanoic acid | 0.21 | |||
Stearic acid | 7.60 | |||
Palmitoleic acid | 0.32 | |||
Oleic acid | 35.20–43.72 | |||
Linoleic | 32.48–44.93 | |||
A. squamosa | Seed (%) | Oleic acid | 41.9 | [87] |
Palmitic acid | 14.7 | |||
Linoleic acid | 26.6 | |||
Stearic acid | 11.3 | |||
Hexadenoic acid | 10–14 | |||
Hepatadecene-(8)-carbonic acid (1) | 29.68 | |||
Cis-vaccenic acid | 10.39 | |||
Heneicosanoic acid | 3.20 | |||
9-octadecenoic acid (Z)-,2,3-dihydroxy propyl ester | 13.33 |
Annona Species | Plant Part | Bioactive Compound | References |
---|---|---|---|
Cyclopeptides | |||
A. muricata | Seed | Annomuricatin A-C | [101,102] |
A. cherimola | Seed | Cherimolacyclopeptide E, herimolacyclopeptide F | [103,104] |
A. squamosa | Seed | Cyclosquamosins A–G, | [105,106,107] |
cyclosquamosin, met-cherimolacyclopeptide B | |||
Peel | Fanlizhicyclopeptide A-B | [108] | |
Alkaloids | |||
A. muricata | Root, bark | Anomurine, anomuricine, atherosperminine, coreximine, coclaurine | [109] |
Stem | Atherospermine, casuarine, 2,5-dihydroxymethyl-3,4,dihydroxypyrrolidine, deoxymannojirimycin, deoxynojirmycin | [109,110] | |
Leaf | Stepharine, coclaurine, coreximine, annonaine, asimilobine, 2,5-dihydroxymethyl-3,4,dihydroxypyrrolidine, deoxymannojirimycin, deoxynojirmycin, swainsonine, (R)-O,O-dimethylcoclaurine, annonamine, R)-4′O-methylcocaurine, S)-narcorydine, xylopine, N-methylcoclaurine, remerine, isoboldine, isolaureline, liriodenine, reticuline, N-methylcoculaurine | [109,110,111,112,113,114] | |
Fruit | Nornuciferine, annonaine, asimilobine | [111,113,114] | |
Peel | Nornuciferin, assimilobin, anonaine, isolaureline | [83] | |
A. cherimola | Leaf | Liriodenine, anonaine, nornuciferine, 1,2- dimethoxy-5,6,6a,7-tetrahydro-4 h, dibenzoquinoline-3,8,9,10-tetraol, asimilobine, pronuciferine | [84] |
Root | Corytenchine, isocoreximine | [115] | |
A. squamosa | Leaf | Reticuline, o-methylarmepavine, annonaine, oxophoebine, lysicamine, n-methylcoclaurine, liriodenine, corydine, lanuginosine, roemerine, corypalmine, sanjoinine, norlaureline, norcodeine, oxalanobie, aporphine | [75,116,117,118] |
Seed | Annonaine, asimilobine, liriodenine, corypalmine, reticuline, nornuciferine | [119] | |
Stem bark | Roemerolidine, N-nitrosoxylopine, duguevalline | [120] | |
A. diversifolia | Seed | Rolliniastatin-2, laherradurin, cherimolin-2 and liriodenine | [88,121] |
Root, Stem bark, leaf | Liriodenine, atherospermidine, lysicamine | [122] | |
Acetogenins | |||
A. muricata | Pulp | Montecristin, epomuricenins A-B, epoxymurin, epomurinins A-B, epomusenins A-B, annonacin, corossolone, muricatin C, muricin, montanacin | [123,124,125,126] |
Leaf | Annocatalin, annohexocin, annomuricin A-E, annomutacin, annonacin, annopentocin A-C, corossolone, gigantetronenin, goniothalamicina, montanacin, muricapentocin, muricatalicin, muricin, muricatalin, muricatocin A-C, murihexocin, muricoreacin, solamin | [82,127,128,129] | |
Seed | Ronbusticin, annomuricatin A, cohibin A-D, donhexocin, muricatenol, murihexol, epomuricenins A-B, corepoxylone, Epoxyrollin B, annoglaxin, annomontacin, annonacin, annoreticuin-9-one, arianacin, corossolina, corossolona, gigantetrocin A-B, goniothalamicina, muricatetrocin A-B, Muricatin A-D, muricin A-I, murisolina, solamin, bullatacilin, bullatacin, gigantecin, annocatacin | [82,89,101,130,131,132,133,134] | |
Root | Cohibin A-B, montecristin, epomuricenins A-B, sabadelin, annonacin | [82,125] | |
Stem bark | Muricatin C | [124] | |
A. cherimola | Pulp | Bullatacin, annonacin | [135] |
Leaf | Molvizarin, cherimolin-1, motrilin, annonacin, annonisin | [136] | |
Seed | Cherimolin, dihydrocherimolin, molvizarin, motrilin, itrabin, jetein, cherimolin-2, almunequin, annomolin, annocherimolin | [137,138] | |
Stem bark | Aromin-A, squamocin | [138] | |
Leaf | Murihexocin C | [139] | |
A. squamosa | Seed | Annotemoyin, squamocin, annoglaxin, epoxyrolin, murisolin, neo- desacetyluvaricin, squamostatin, annosquamins, bullatacin, annosquacin, annosquatin, annonareticin, motrilin, solamin, squadiolin, squamoxinone, squamostanin, uvarigrandin, squamostolide, tripoxyrollin, uvariamicin | [75,140,141,142] |
Stem bark | 4-deoxyannoreticuin, cis-4-deoxyannoreticuin, (2-4-cis and trans)-squamoxinone, annoreticuin-9-one, bullatacin, molvizarin, mosin, parviflorin, squamotacin | [75,143] | |
A. macroprophyllata | Seed | Laherradurin, rolliniastin-2, and cherimolin-2 | [89] |
Activity/Annona Species | Plant Part | Bioactive | Dose/Concentration | Model Assay | Effect | References |
---|---|---|---|---|---|---|
Cytotoxicity | ||||||
A. muricata | Leaf | Annonacin | 85 nM | Mice induced a skin tumorogenesis | To reduce the tumor incidence, tumor burden, and tumor volume | [147] |
Acetogenin-rich fraction | 100 and 200 mg/kg for 7 days | Rats induced benign prostatic hyperplasia (PSA) | The fractions (200 mg/kg) significantly reduced the PSA level | [148] | ||
Root-bark, fruit, leaf | Ethyl acetate extract | 50 µg/mL | MCF-10A cell line (breast) | The fractions had the highest anticancer abilities | [149] | |
Stem bark | Annonacin and ethyl acetate extract | IC50 0.1 μM and 55.501 μg/mL | DU-145 prostate carcinoma cells | Annonacin and extract displayed selective and potent cytotoxicity | [150] | |
A. cherimola | Seed | Annomolin, annocherimolin | A-549 (lung), MCF-7 (breast), HT-29 (colon), A-498 (kidney), PC-3 (prostate) and MIA PaCa-2 (pancreas) cell lines | Potent cytotoxicity against all cell lines | [137] | |
Ethanolic extract | IC50 23.20 μg/mL | Colorectal cancer cell lines: T84, HCT-15, SW480 and HT-29, cancer stem cells | Potential cytotoxic activity on T-81 and HCT-15 resistant cell lines | [151] | ||
Leaf | Ethanolic extract | IC50 390.20 μg/mL | Breast cancer cell lines: MDA-MB-231 and MCF-7 | Selective antiproliferative and pro-apoptotic activities | [152] | |
A. squamosa | Stem bark | Bullatacin | IC50 of 2.47 × 10−7 µg/mL | A-549, HT-29, MCF-7, A-498, PC3 and PACA-2 cell lines | Selective cytotoxic activity against MCF-7 cells | [142] |
Seed | Acetogenins | IC50 ranged from 2.2 × 10−1 to 8.3 × 10−3 µg/mL | HeLa, MCF-7, A-549, Hep-G2, SMMC-7721 and MKN-45 cell lines | Selective cytotoxic activity against MCF-7 and A-549 cells | [141] | |
Leaf | Methanolic extract | IC50 ranged from 1.1 to 2.1 µg/mL | Human immortalized line of T lymphocyte (Jurkat), MCF-7, HL60, and HCT-116 | Leaf extract was more active against MCF-7 cells, likewise for seed extract against Jurkat and HL60 cells | [119] | |
Seed, peel, pulp | Aqueous extract | IC50 7.31 ± 0.03 and 15.99 ± 1.25 µg/mL | Cancer cell lines colon (Caco-2), prostate (PC3), liver (HepG-2), and breast (MCF-7) | Seed extracts had the lowest IC50 values for PC-3 and MCF-7 cancer cell lines | [96] | |
A. macroprophyllata | Seed | Cherimolin-2 | IC50 of 0.5 µg/mL for SW-480 and for HeLa 0.05 µg/mL. In vivo doses 500 mg/kg body weight, 20 days | HeLa and SW-480 cell line and rats injected with HeLa (1 × 106) or SW-480 (5 × 106) cells | Size reduction of HeLa tumor (43%), and 16% of SW-480 tumor | [88] |
Laherradurin | IC50 of 0.15 µg/mL for HeLa and SW-480. In vivo doses 500 mg/kg body weight 20 days | HeLa and SW-480 cell line and rats injected with HeLa (1 × 106) or SW-480 (5 × 106) cells | Size reduction of HeLa tumor (64%) and SW-480 tumor (60%) | [88] | ||
Hypoglycemic activity | ||||||
Leaf | Aqueous extract | 100 mg/kg for 2 weeks | Streptozotocin-induced diabetic rats, | Significant reduction of blood glucose levels and protective action on pancreatic β-cells | [153] | |
A. muricata | Dry extract | 100 mg/kg/day for 4 weeks | Streptozotocin-induced diabetic rats. | The dry extract improves behavioral alterations and protects testis in diabetic animals | [154] | |
Steam bark | Ethanolic extract | 150 and 300 mg/kg for 2 weeks | Alloxan-induced diabetic male albino rats | [155] | ||
A. cherimola | Leaf | Ethanolic extract | 300 mg/kg, one week | Alloxan-induced type 2 diabetic (AITD) | Attenuated postprandial hyperglycemia | [156] |
Aqueous extract (infusion) (1.5 g/mL) | 300 mg/kg | Streptozocin-induced diabetic mice | Reduction of the blood glucose level, glycated hemoglobin, cholesterol, and triacylglycerols | [157] | ||
A. squamosa | Leaf | Aqueous extract | 300 mg/kg body weight | Streptozotocin-induced Wistar rats | Decreased glucose and increased insulin sensitivity | [158] |
Ethanolic extract | 100 mg/kg body weight | Streptozotocin-induced rats | Glycemia decreased as well as glycated hemoglobin, creatinine, and urea | [159] | ||
Root | Aqueous extract | 500 mg/kg body weight | Streptozotocin-induced hyperglycemic rats | A significant reduction of glycemia, 6 h after oral administration | [160] | |
Leaf and peel | Aqueous extract | 250 mg/kg body weight | Streptozotocin-induced diabetic rats | Improvement of the glycemia and lipid profile | [161] | |
A. macroprophyllata | Leaf | Ethanolic extract | 200 mg/kg body weight | Alloxan-induced diabetic Balb-c mice | A significant decrease in postprandial hyperglycemia | [162] |
Aqueous extract | 300 mg/kg body weight | Healthy rats | Reduction of glycemia at a dose-dependent manner | [163] | ||
Anti-inflammatory activity | ||||||
A. muricata | Fruit | Aqueous extract | 50, 100 and 200 mg/kg | Carrageenan-induced paw edema rats and xylene-induced-ear edema rats | Significant anti-inflammatory activity on paw edema and ear edema | [164] |
Leaf | Aqueous extract | 100 mg/kg body weight | Female Balb/c albino mice injected with Escherichia fergusonii | The extract minimized the inflammation by decreasing the expression levels of IL-1β and TNF-α | [165] | |
Ethanolic extract | 100, 200, and 400 mg/kg orally for 7 days | Rectoanal tissue from Swiss mice | All three doses show significant anti-inflammatory effects on hemorrhoidal tissue | [166] | ||
A. cherimola | Leaf | Ethanolic extracts | 100 mg/kg | Rats (Leukocyte migration to the peritoneal cavity and Subcutaneous air pouch test) | The inhibitory effect of the ethanolic extract on leukocytes migration was 63.8 and 73.16% | [167] |
A. squamosa | Root | Ethanolic extract | 400 mg/kg body weight | Carrageenan-induced paw edema rats | Inhibition (54%) of edema inflammation at 400 mg/kg | [168] |
Stem bark | Caryophyllene oxide | 25 mg/kg body weight | Acetic acid-induced Swiss albino rats | Inhibition of inflammation (75% ) at 25 mg/kg | [169] | |
18-acetoxyent-kaur-16-ene | 25 mg/kg body weight | Acetic acid-induced rats | Inhibition of inflammation 62%) at 25 mg/kg | [170] |
Technology/Treatment | Genus Annona | Effect | References |
---|---|---|---|
Aqueous extract of coconut mesocarp + commercial chitosan | Annona muricata L. | Control of Rhizopus stolonifera | [182] |
Electrolyzed solution with neutral pH | Annona muricata L. | Sporicidal activity | [183] |
Hydrothermal, fungicidal, and wax treatment | Annona muricata L. | Browning control | [184] |
Edible mucilage coating | Annona muricata L. | Preservation of the physicochemical characteristics and extending the shelf life (2 extra days) | [185] |
1-Methylcyclopropene | Annona muricata L. | Preservation of physicochemical characteristics | [186] |
Chitosan coating | Annona muricata L. | Anthracnose control | [187] |
Chitosan coating | Annona muricata L. | Control of physicochemical, microbiological, and sensory characteristics | [188] |
Cold storage | Annona muricata L. | Increase the days of shelf life of the fruit (2 extra days) | [189] |
Bacillus atrophaeus strain B5 | Annona muricata L. | Biocontrol of postharvest anthracnose | [190] |
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Hernández Fuentes, L.M.; Montalvo González, E.; García Magaña, M.d.L.; Anaya Esparza, L.M.; Nolasco González, Y.; Villagrán, Z.; González Torres, S.; Velázquez Monreal, J.J.; Morelos Flores, D.A. Current Situation and Perspectives of Fruit Annonaceae in Mexico: Biological and Agronomic Importance and Bioactive Properties. Plants 2022, 11, 7. https://doi.org/10.3390/plants11010007
Hernández Fuentes LM, Montalvo González E, García Magaña MdL, Anaya Esparza LM, Nolasco González Y, Villagrán Z, González Torres S, Velázquez Monreal JJ, Morelos Flores DA. Current Situation and Perspectives of Fruit Annonaceae in Mexico: Biological and Agronomic Importance and Bioactive Properties. Plants. 2022; 11(1):7. https://doi.org/10.3390/plants11010007
Chicago/Turabian StyleHernández Fuentes, Luis M., Efigenia Montalvo González, Maria de Lourdes García Magaña, Luis M. Anaya Esparza, Yolanda Nolasco González, Zuamí Villagrán, Sughey González Torres, José Joaquín Velázquez Monreal, and David Antonio Morelos Flores. 2022. "Current Situation and Perspectives of Fruit Annonaceae in Mexico: Biological and Agronomic Importance and Bioactive Properties" Plants 11, no. 1: 7. https://doi.org/10.3390/plants11010007
APA StyleHernández Fuentes, L. M., Montalvo González, E., García Magaña, M. d. L., Anaya Esparza, L. M., Nolasco González, Y., Villagrán, Z., González Torres, S., Velázquez Monreal, J. J., & Morelos Flores, D. A. (2022). Current Situation and Perspectives of Fruit Annonaceae in Mexico: Biological and Agronomic Importance and Bioactive Properties. Plants, 11(1), 7. https://doi.org/10.3390/plants11010007