Armeria maritima (Mill.) Willd. Flower Hydromethanolic Extract for Cucurbitaceae Fungal Diseases Control
Abstract
:1. Introduction
2. Results
2.1. Vibrational Spectroscopy Characterization
2.2. GC–MS Characterization
2.3. Antifungal Activity of the Extract
2.3.1. In Vitro Antifungal Activity
2.3.2. Ex Situ Antifungal Activity
3. Discussion
3.1. On the Phytochemical Profile Obtained by GC–MS
3.2. On the Antifungal Activity and Mode of Action
3.3. Efficacy Comparisons
3.3.1. Comparison with Conventional Fungicides
3.3.2. Comparison with Other Extracts Tested In Vitro against the Phytopathogens under Study
3.3.3. Comparison with Other Extracts Tested Ex Situ for Cucumber Protection
3.4. Limitations of the Study and Further Research
4. Materials and Methods
4.1. Plant Material and Chemicals
4.2. Phytopathogen Isolates
4.3. Preparation of Armeria Extract, Chitosan Oligomers, and Conjugate Complexes
4.4. Physicochemical Characterization
4.5. In Vitro Antifungal Activity Assessment
4.6. Post-Harvest Protection Test in Cucumber
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Sample Availability
References
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Flowers | Root | Stem | Assignment |
---|---|---|---|
3290 | 3282 | 3355 | OH group in phenolic compounds |
2918 | 2921 | 2919 | O−H stretching |
2850 | 2851 | 2850 | –CH2 symmetric stretching (cutine and wax); CH2–(C6)– bending (cellulose) |
1732 | 1726 | C=O stretching of alkyl ester | |
1651 | C=O (amide I) | ||
1633 | 1620 | 1639 | skeletal vibration due to aromatic C=C ring stretching and C=O stretching |
1605 | C=C stretching | ||
1545 | 1546 | aromatic C=C stretching | |
1515 | 1517 | aromatic skeletal | |
14,351,416 | 1445 | 14,431,414 | symmetric aromatic ring stretching vibration (C=C ring);aromatic skeletal combined with C−H in-plane deformation and stretching |
1367 | 1344 | 1371 | aliphatic C−H stretching in methyl and phenol OH |
1308 | 1321 | C−H vibration of the methyl group | |
1240 | 1238 | 1236 | aromatic ring−O−aromatic ring stretching |
1201 | present in hemicelluloses | ||
1162 | 1145 | 1152 | C-O-C asymmetric stretching in cellulose I and cellulose II |
1103 | in-plane =C−H bending/C=C stretching | ||
1030 | 1034 | 1033 | C–O stretching/O−H out plane bending |
896 | 919 | β-glycosidic linkages (glucose units of cellulose chains) |
RT (min) | Peak Area (%) | Assignment | Qual |
---|---|---|---|
5.3273 | 1.6888 | 2-Furancarboxaldehyde, 5-methyl- | 93 |
6.5084 | 0.3951 | Piperazine, 1,4-dimethyl- | 52 |
6.5618 | 4.4740 | Benzeneacetaldehyde | 93 |
6.7815 | 0.3599 | 2,5-Dimethyl-4-hydroxy-3(2H)-furanone | 62 |
6.9951 | 0.3635 | Thiazole | 43 |
7.3572 | 0.4867 | Cyclopropanecarboxylic acid, 1-amino- | 59 |
8.1110 | 1.7736 | 4H-Pyran-4-one, 2,3-dihydro-3,5-dihydroxy-6-methyl- | 91 |
8.4077 | 0.2368 | Benzoic acid | 55 |
9.1615 | 2.5799 | Benzofuran, 2,3-dihydro- | 83 |
10.5563 | 2.3649 | 2-Methoxy-4-vinylphenol | 95 |
11.1439 | 0.6006 | Methyl 3-methoxyamino-propanoate | 38 |
12.1826 | 8.4919 | 2,1,3-Benzothiadiazole/2-trifluoromethyl imidazole | 53 |
12.2538 | 0.7550 | 2,2′-Bipyridine | 92 |
13.0669 | 2.7909 | 3,4-Altrosan | 49 |
13.6189 | 0.1442 | 1-Pyrrolidinyloxy, 3-amino-2,2,5,5-tetramethyl- | 53 |
13.7376 | 1.3464 | 3-Hydroxy-4-methoxybenzoic acid | 95 |
13.8029 | 0.2216 | 3-Piperidinone, 1,6-dimethyl- | 64 |
14.1590 | 5.8153 | β-D-Glucopyranoside, methyl | 58 |
15.7378 | 0.5604 | 4-((1E)-3-Hydroxy-1-propenyl)-2-methoxyphenol | 46 |
15.7912 | 1.5928 | 2-Propenoic acid, 3-(4-hydroxyphenyl)-, methyl ester | 98 |
15.8625 | 1.0835 | Tetradecanoic acid | 98 |
16.5450 | 0.8155 | Benzoic acid, 4-hydroxy-3,5-dimethoxy- | 98 |
16.7884 | 0.5167 | 2-Propenoic, 3-(4-hydroxy-3-methoxyphenyl)-, methyl ester | 99 |
16.9071 | 0.5716 | Pentadecanoic acid | 96 |
17.0851 | 1.0764 | 2-Propenoic acid, 3-(4-hydroxy-3-methoxyphenyl)- | 94 |
17.1326 | 0.4642 | 2-Tetradecene, (E)- | 90 |
17.4175 | 4.0260 | 1,5-Heptadiene, 3,3,6-trimethyl- | 38 |
17.5896 | 0.9559 | Pentadecanoic acid, 14-methyl-, methyl ester | 97 |
17.7262 | 1.1349 | 5-Undecene | 46 |
17.9576 | 18.0487 | n-Hexadecanoic acid (or palmitic acid) | 99 |
18.3019 | 5.3442 | 3-(3,4-Dihydroxy-phenyl)-acrylic acid ethyl ester | 91 |
19.2753 | 0.5834 | 11-Octadecenoic acid, methyl ester | 99 |
19.6195 | 14.4270 | 9-Octadecenoic acid, (E)-//Oleic acid | 99 |
19.8154 | 9.0166 | Octadecanoic acid (or stearic acid) | 99 |
20.2605 | 1.6119 | 4-Methoxybenzoic acid, 2,4,5-trichlorophenyl ester | 43 |
20.7769 | 0.4864 | 7-Butyl-3,4,5,6(2H)-tetrahydroazepine | 49 |
20.8956 | 0.5923 | Isophthalic acid, di(but-3-yn-2-yl) ester | 35 |
24.7179 | 0.6977 | Octabenzone | 98 |
25.0919 | 1.5047 | Supraene | 98 |
Treatment | EC | F. equiseti | F. oxysporum f. sp. niveum | M. phaseolina | N. falciformis | N. keratoplastica | S. sclerotiorum |
---|---|---|---|---|---|---|---|
COS | EC50 | 867.8 | 455.9 | 1151.7 | 721.8 | 677.5 | 864.3 |
EC90 | 1350.4 | 1296.4 | 1420.5 | 1130.2 | 1295.4 | 1344.8 | |
A. maritima flower extract | EC50 | 448.0 | 387.4 | 413.2 | 463.4 | 482.2 | 13.5 |
EC90 | 832.4 | 660.1 | 664.2 | 1053.1 | 845.1 | 235.6 | |
Hexadecanoic acid | EC50 | 297.1 | 275.9 | 156.0 | 268.3 | 230.0 | 120.3 |
EC90 | 422.8 | 472.8 | 278.5 | 501.8 | 346.5 | 164.0 | |
9-octadecenoic acid | EC50 | 213.7 | 195.8 | 213.8 | 111.7 | 46.8 | 62.8 |
EC90 | 347.2 | 354.3 | 238.7 | 242.0 | 163.2 | 110.0 | |
Octadecanoic acid | EC50 | 231.3 | 202.6 | 269.7 | 126.4 | 35.5 | 27.7 |
EC90 | 552.6 | 503.3 | 385.7 | 462.6 | 214.5 | 137.2 | |
COS–A. maritima | EC50 | 320.3 | 205.7 | 308.1 | 444.1 | 442.7 | 129.2 |
EC90 | 461.5 | 452.4 | 482.5 | 865.2 | 683.4 | 165.9 | |
COS– hexadecanoic acid | EC50 | 110.9 | 114.0 | 36.7 | 113.9 | 103.6 | 29.3 |
EC90 | 210.8 | 224.6 | 136.4 | 245.8 | 168.7 | 61.5 | |
COS– 9-octadecenoic acid | EC50 | 121.5 | 107.8 | 83.2 | 79.5 | 29.7 | 21.1 |
EC90 | 199.5 | 218.9 | 127.8 | 91.0 | 74.8 | 62.4 | |
COS– octadecanoic acid | EC50 | 109.3 | 102.8 | 131.1 | 86.8 | 9.3 | 25.4 |
EC90 | 256.3 | 231.4 | 193.1 | 101.9 | 48.9 | 61.2 |
Treatment | EC | F. equiseti | F. oxysporum f. sp. niveum | M. phaseolina | N. falciformis | N. keratoplastica | S. sclerotiorum |
---|---|---|---|---|---|---|---|
COS– A. maritima | EC50 | 1.84 | 2.04 | 1.97 | 1.27 | 1.27 | 2.34 |
EC90 | 2.34 | 1.93 | 1.88 | 1.36 | 1.50 | 2.42 | |
COS– hexadecanoic acid | EC50 | 3.99 | 3.02 | 7.49 | 3.43 | 3.31 | 7.21 |
EC90 | 3.26 | 3.09 | 3.41 | 2.96 | 3.24 | 4.75 | |
COS– 9-octadecenoic acid | EC50 | 2.82 | 2.54 | 4.33 | 2.43 | 2.95 | 5.55 |
EC90 | 2.84 | 2.54 | 3.20 | 4.50 | 3.88 | 3.26 | |
COS– octadecanoic acid | EC50 | 3.34 | 2.73 | 3.33 | 2.43 | 7.25 | 2.11 |
EC90 | 3.17 | 3.13 | 3.14 | 4.50 | 7.53 | 4.07 |
Commercial Fungicide | Pathogen | Radial Growth of Mycelium (mm) | Inhibition (%) | |||
---|---|---|---|---|---|---|
Control (PDA) | Rd/10 | Rd * | Rd/10 | Rd * | ||
Azoxystrobin | F. equiseti | 75.0 | 50.0 | 46.7 | 33.3 | 37.8 |
F. oxysporum f. sp. niveum | 75.0 | 45.0 | 40.0 | 40.0 | 46.7 | |
M. phaseolina | 75.0 | 38.3 | 16.7 | 48.9 | 77.8 | |
N. falciformis | 75.0 | 43.3 | 28.3 | 42.2 | 62.2 | |
N. keratoplastica | 75.0 | 10.0 | 0.0 | 86.7 | 100.0 | |
S. sclerotiorum | 75.0 | 14.0 | 9.0 | 81.3 | 88.0 | |
Mancozeb | F. equiseti | 75.0 | 70.0 | 25.0 | 6.7 | 66.7 |
F. oxysporum f. sp. niveum | 75.0 | 0.0 | 0.0 | 100.0 | 100.0 | |
M. phaseolina | 75.0 | 0.0 | 0.0 | 100.0 | 100.0 | |
N. falciformis | 75.0 | 0.0 | 0.0 | 100.0 | 100.0 | |
N. keratoplastica | 75.0 | 0.0 | 0.0 | 100.0 | 100.0 | |
S. sclerotiorum | 75.0 | 0.0 | 0.0 | 100.0 | 100.0 | |
Fosetyl-Al | F. equiseti | 75.0 | 75.0 | 30.0 | 0.0 | 20.0 |
F. oxysporum f. sp. niveum | 75.0 | 66.7 | 0.0 | 11.1 | 100.0 | |
M. phaseolina | 75.0 | 75.0 | 0.0 | 0.0 | 100.0 | |
N. falciformis | 75.0 | 61.7 | 0.0 | 17.8 | 100.0 | |
N. keratoplastica | 75.0 | 66.7 | 0.0 | 11.1 | 100.0 | |
S. sclerotiorum | 75.0 | 75.0 | 13.3 | 0.0 | 82.2 |
Treatment | Day 1 | Day 2 | Day 3 | Day 4 | Day 5 | Day 6 | Day 7 |
---|---|---|---|---|---|---|---|
C− | 1.01 ± 0.00 a | 1.00 ± 0.00 a | 0.99 ± 0.00 ab | 0.96 ± 0.00 ab | 0.91 ± 0.00 ab | 0.89 ± 0.01 a | 0.85 ± 0.01 a |
C+ | 1.01 ± 0.01 a | 1.00 ± 0.01 a | 0.93 ± 0.01 b | 0.91 ± 0.01 b | 0.87 ± 0.02 b | 0.59 ± 0.04 b | 0.43 ± 0.05 b |
MIC | 1.01 ± 0.00 a | 1.00 ± 0.00 a | 0.99 ± 0.00 a | 0.96 ± 0.00 ab | 0.91 ± 0.01 ab | 0.90 ± 0.01 a | 0.84 ± 0.01 a |
MIC×2 | 1.02 ± 0.03 a | 1.01 ± 0.03 a | 1.00 ± 0.03 a | 0.97 ± 0.03 a | 0.92 ± 0.03 ab | 0.92 ± 0.03 a | 0.82 ± 0.10 a |
MIC×4 | 1.03 ± 0.04 a | 1.03 ± 0.04 a | 1.02 ± 0.04 a | 0.98 ± 0.04 a | 0.94 ± 0.04 a | 0.93 ± 0.04 a | 0.93 ± 0.08 a |
Pathogen | Source/Extraction Medium | Plant | Efficacy | Ref. |
---|---|---|---|---|
F. equiseti | Aqueous ammonia | Tamarix gallica bark | MIC = 750 µg·mL−1 | [69] |
Commercial essential oil | Zataria multiflora | MIC = 99–145 µg·mL−1 | [70] | |
Heracleum persicum | MIC = 795–1180 µg·mL−1 | |||
Pinaceae | MIC = 163–176 µg·mL−1 | |||
Cuminum cyminum | MIC = 75–99 µg·mL−1 | |||
Foeniculum vulgare | MIC = 63–69 µg·mL−1 | |||
Oil cake extracts at 1–3% | Brassica napus | IR = 43.6–59.1% | [71] | |
Cocos nucifera | IR = 7.6–22.4% | |||
Sesame indicum | IR = 49.4–56.1% | |||
Glycine max | IR = 0.4–5.9% | |||
Essential oil | Piper auritum aerial parts | MIC50 = 9000 µg·mL−1 | [72] | |
Ethanol extract | Emblica officinalis fruits | IZ = 9.5 mm | [73] | |
Acetone extract | IZ = 10 mm | |||
Ethanol extract | Plumbago zeylanica roots | MIC = 250 µg·mL−1 | [74] | |
Aqueous extract at 25% | Acacia nilotica leaves | IR = 67% | [75] | |
Achras zapota leaves | IR = 44.8% | |||
Datura stramonium leaves | IR = 87.3% | |||
E. officinalis leaves | IR = 75.8% | |||
Eucalyptus globulus leaves | IR = 62.0% | |||
Lawsonia inermis leaves | IR = 78.3% | |||
Mimusops elengi leaves | IR = 85.8% | |||
Peltophorum pterocarpum leaves | IR = 74.3% | |||
Polyalthia longifolia leaves | IR = 40.5% | |||
Prosopis juliflora leaves | IR = 76.8% | |||
Punica granatum leaves | IR = 77.5% | |||
Syzygium cumini leaves | IR = 68.8% | |||
Aqueous extract | Filipendula spp. flowers | IR = 100% | [76] | |
Allium sativum | IR = 92.2% | |||
F. oxysporum spp. | Aqueous extract at 5, 10, and 20% | Azadirachta indica leaves | n.a. | [77] |
Parthenium hysterophorus leaves + flowers | IR = 2.6–15.9% | |||
Momordica charantia leaves | IR = 14.4–24.4% | |||
A. sativum cloves | IR = 52.6–63.3% | |||
Eucalyptus globules leaves | IR = 34.3–61.8% | |||
Calotropis procera leaves | n.a. | |||
Aloe vera leaves | IR = 16.6% | |||
Beta vulgaris root | IR = 6.3–10.3% | |||
D. stramonium leaves | IR = 61.1% | |||
Aqueous extract at 1% | P. granatum fruits | IR = 78% | [78] | |
Propanol extract at 1% | IR = 62% | |||
Hexane extract | Cestrum nocturnum flowers | MIC = 1000 µg·mL−1 | [79] | |
Chloroform extract | MIC = 1000 µg·mL−1 | |||
Ethyl acetate extract | MIC = 500 µg·mL−1 | |||
Methanol extract | MIC = 500 µg·mL−1 | |||
Crude extract at 5, 10, and 20% | A. indica leaves | IR = 24.1–62.0% | [80] | |
Ocimum sanctum leaves | IR = 7.0–17.0% | |||
Datura metel leaves | IR = 10.1–34.2% | |||
Cassia alata leaves | IR = 46.8–74.7% | |||
Asparagus racemosus roots | IR = 44.3–57.0% | |||
A. sativum bulbs | IR = 17.6–34.2% | |||
Zingiber officinale tubers | IR = 23.7–39.5% | |||
Ethanol extract | Flourensia microphylla leaves | MIC = 1500 µL·L−1 | [81] | |
F. cernua leaves | MIC = 1500 µL·L−1 | |||
F. retinophylla leaves | MIC = 1500 µL·L−1 | |||
Aqueous extract at 5–50% | Moringa oleifera leaves | IR = 43.4–100% | [82] | |
M. oleifera roots | IR = 48.8–100% | |||
M. oleifera pud coats | IR = 36–100% | |||
Commercial essential oil | Z. multiflora | MIC = 77–183 µg·mL−1 | [70] | |
H. persicum | MIC = 753–2250 µg·mL−1 | |||
Pinaceae | MIC = 113–147 µg·mL−1 | |||
C. cyminum | MIC = 70–145 µg·mL−1 | |||
F. vulgare | MIC = 77–94 µg·mL−1 | |||
Essential oil | P. auritum aerial parts | MIC50 = 6000–9000 µg·mL−1 | [72] | |
Aqueous extract at 25% | A. nilotica leaves | IR = 82% | [75] | |
A. zapota leaves | IR = 34.8% | |||
D. stramonium leaves | IR = 67.5% | |||
E. officinalis leaves | IR = 79.5% | |||
E. globulus leaves | IR = 59.3% | |||
L. inermis leaves | IR = 82.0% | |||
M. elengi leaves | IR = 86.0% | |||
P. pterocarpum leaves | IR = 53.3% | |||
P. longifolia leaves | IR = 36.3% | |||
P. juliflora leaves | IR = 80.3% | |||
P. granatum leaves | IR = 73.8% | |||
S. cumini leaves | IR = 69.5% | |||
Aqueous extract | Filipendula spp. flowers | IR = 95.9% | [76] | |
A. sativum | IR = 81.4% | |||
Ethanolic extract | Mentha spicata | MIC = 5% | [83] | |
Aqueous extract | A. sativum leaves | MIC = 7000 µg·mL−1 | [84] | |
M. phaseolina | Aqueous extract at 5, 10, and 20% | A. indica leaves | n.a. | [77] |
P. hysterophorus leaves + flowers | n.a. | |||
M. charantia leaves | n.a. | |||
A. sativum cloves | IR = 100% | |||
E. globules leaves | n.a. | |||
C. procera leaves | n.a. | |||
A. vera leaves | n.a. | |||
B. vulgaris root | n.a. | |||
D. stramonium leaves | IR = n.a –57.7% | |||
Aqueous extract at 5–50% | M. oleifera leaves | IR = 17.8–82.2% | [82] | |
M. oleifera roots | IR = 20–87.4% | |||
M. olifera pud coats | IR = 13.8–82.2% | |||
Chloroform extract | Ageratum conyzoides leaves | n.a. | [85] | |
Antigonon leptopus leaves | ||||
Chromolaena odorata leaves | ||||
Oxalis corniculata leaves | ||||
Passiflora foetida leaves | ||||
Methanol extract | A. conyzoides leaves | MIC = 1250 µg·mL−1 | ||
A. leptopus leaves | MIC = 625 µg·mL−1 | |||
C. odorata leaves | MIC = 2500 µg·mL−1 | |||
O. corniculata leaves | MIC = 78 µg·mL−1 | |||
P. foetida leaves | MIC = 1250 µg·mL−1 | |||
Aqueous extract at 5–20% | Citrus aurantifolia leaves | IR = 75.6–96.7% | [86] | |
Ethanol extract | E. officinalis fruits | n.a. | [73] | |
Acetone extract | ||||
Ethanol extract | P. zeylanica roots | MIC = 500 µg·mL−1 | [74] | |
N. keratoplastica | Essential oil | Trachyspermum ammi seeds | n.a. | [87] |
Essential oil | Kaempferia parviflora rhizome | IZ = 17–18 mm | [88] | |
Essential oil | Pogostemon cablin flowers + leaves | n.a. at 500 µg·mL−1 | [89] | |
Essential oil | Origanum vulgare subsp. hirtum | MIC = 800 µg·mL−1 | [90] | |
S. sclerotiorum | Hexane extract | C. nocturnum flowers | MIC = 1000 µg·mL−1 | [79] |
Chloroform extract | MIC = 500 µg·mL−1 | |||
Ethyl acetate extract | MIC = 250 µg·mL−1 | |||
Methanol extract | MIC = 500 µg·mL−1 | |||
Essential oils at 1, 2.5, and 5% | Thymus vulgaris | n.a. | [91] | |
Nigella sativa | n.a. | |||
Origanum majorana | MIC = 2.5% | |||
Syzygium aromaticum | MIC = 2.5% | |||
Salvia rosmarinus | n.a. | |||
Essential oils at 20% | Ocimum basilicum | IR = 4.1% | [92] | |
A. sativum | IR = 28.2% | |||
Cymbopogon citratus | IR = 9.1% | |||
Nerium oleander | IR = 14.1% | |||
A. indica | IR = 35.5% | |||
Allium cepa | IR = 16.9% | |||
Essential oil | Z. officinale | MIC = 1000 µg·mL−1 | [93] | |
Aqueous extracts | Trachystemon orientalis leaves | MIC = 7% | [94] | |
T. orientalis flowers | MIC = 1% | |||
Crude extracts | Rosmarinus officinalis leaves | MIC = 10% | [95] | |
Salvia fructicosa leaves | MIC = 20% | |||
Ethanol extract | M. spicata | MIC = 5% | [83] | |
Aqueous extract | A. sativum leaves | MIC = 5000 µg·mL−1 | [84] |
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Sánchez-Hernández, E.; Martín-Ramos, P.; Navas-Gracia, L.M.; Martín-Gil, J.; Garcés-Claver, A.; Flores-León, A.; González-García, V. Armeria maritima (Mill.) Willd. Flower Hydromethanolic Extract for Cucurbitaceae Fungal Diseases Control. Molecules 2023, 28, 3730. https://doi.org/10.3390/molecules28093730
Sánchez-Hernández E, Martín-Ramos P, Navas-Gracia LM, Martín-Gil J, Garcés-Claver A, Flores-León A, González-García V. Armeria maritima (Mill.) Willd. Flower Hydromethanolic Extract for Cucurbitaceae Fungal Diseases Control. Molecules. 2023; 28(9):3730. https://doi.org/10.3390/molecules28093730
Chicago/Turabian StyleSánchez-Hernández, Eva, Pablo Martín-Ramos, Luis Manuel Navas-Gracia, Jesús Martín-Gil, Ana Garcés-Claver, Alejandro Flores-León, and Vicente González-García. 2023. "Armeria maritima (Mill.) Willd. Flower Hydromethanolic Extract for Cucurbitaceae Fungal Diseases Control" Molecules 28, no. 9: 3730. https://doi.org/10.3390/molecules28093730