Combined Effect of the Potassium Dose and Plant Biofertilization by Acinetobacter calcoaceticus on the Growth, Mineral Content, Nutritional Quality, Antioxidant Activity, and Metabolomic Features of Tomatillo Fruits (Physalis ixocarpa Brot.)
Abstract
:1. Introduction
2. Results
2.1. Mineral Content in Plants
2.2. Plant Physiological Parameters
2.3. Plant Growth
2.4. Production Yield
2.5. Quality Characteristics of the Harvested Tomatillo Fruits
2.6. Mineral Content in Tomatillo Fruit
2.7. Phenols Content and Antioxidant Capacity in Tomatillo Fruits
2.8. Multivariate Analysis
2.9. Untargeted and Targeted Metabolomics
3. Discussion
3.1. Effect on Mineral Content in Plant
3.2. Effect on Plant Physiology
3.3. Plant Growth Parameters
3.4. Fruit Yield
3.5. Fruit Nutritional Quality
3.6. Phenolic Compounds and Antioxidant Activity
3.7. PCA Multivariate Analysis
3.8. Metabolomic Analyses
4. Conclusions
5. Materials and methods
5.1. Experimental Site and Design
5.2. Rhizobacterial Inoculant
5.3. Agronomic Parameters
5.4. Physicochemical Parameters of Tomatillo Fruits
5.5. Fruit Extraction for Bioactive and Metabolomic Analyses
5.6. Total Phenolic Content and Antioxidant Capacity
5.7. Metabolomic Analyses of Fruit Extracts
5.7.1. Untargeted Metabolomics
5.7.2. Phenolics Targeted Metabolomics
5.8. Determination of Mineral Elements
5.9. Statistical Analysis
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Treatment 1 | K | P | Ca | Na | Mg | Mn |
---|---|---|---|---|---|---|
KF100 | 25.9 ± 4.61 abc | 0.79 ± 0.13 cd | 13.2 ± 0.9 bc | 4.1 ± 0.4 cd | 6.1 ± 0.25 de | 0.10 ± 0.005 bcd |
KF75 | 21.4 ± 3.31 abc | 0.61 ± 0.12 de | 14.8 ± 1.2 ab | 6.1 ± 0.9 b | 7.3 ± 0.35 bc | 0.09 ± 0.007 cde |
KF50 | 27.9 ± 2.37 a | 1.43 ± 0.12 b | 12.9 ± 0.7 bc | 4.8 ± 0.4 bc | 7.7 ± 0.17 b | 0.07 ± 0.003 ef |
KF0 | 20.0 ± 2.41 c | 0.93 ± 0.01 c | 15.5 ± 0.4 a | 4.6 ± 0.2 bc | 8.7 ± 0.19 a | 0.13 ± 0.004 a |
KB100 | 20. 5 ± 1.13 bc | 0.51 ± 0.13 e | 11.9 ± 1.4 c | 8.0 ± 0.7 a | 6.7 ± 0.61 cd | 0.08 ± 0.007 de |
KB75 | 20.8 ± 0.82 bc | 0.48 ± 0.05 e | 11.2 ± 0.5 c | 4.5 ± 0.3 bc | 6.6 ± 0.14 de | 0.07 ± 0.003 f |
KB50 | 22.3 ± 0.38 abc | 2.13 ± 0.03 a | 12.7 ± 0.5 bc | 4.0 ± 0.7 cd | 5.7 ± 0.09 e | 0.10 ± 0.003 bc |
KB0 | 27.1 ± 1.27 ab | 1.23 ± 0.03 b | 16.0 ± 0.1 a | 2.8 ± 0.7 d | 8.7 ± 0.07 a | 0.11 ± 0.001 b |
Treatment 1 | Photosynthesis (µmol CO2/m2 s) 1 | Chlorophyll (mmol/m2) | Dry Weight (g) | Plant Height (cm) | Stem Thickness (mm) |
---|---|---|---|---|---|
KF100 | 16.1 ± 4.0 a | 134.9 ± 3.4 bc | 58.0 ± 1.2 d | 111.2 ± 8.2 b | 10.7 ± 0.1 a |
KF75 | 12.4 ± 3.3 a | 125.1 ± 13.8 c | 42.6 ± 1.4 f | 106.2 ± 7.7 b | 10.2 ± 1.0 a |
KF50 | 13.2 ± 2.6 a | 133.1 ± 6.2 bc | 53.2 ± 1.4 e | 112.8 ± 9. 7 b | 12.1 ± 0.8 a |
KF0 | 12.3 ± 2.7 a | 129.9 ± 11.6 bc | 61.1 ± 0.9 c | 97.7 ± 4.9 b | 10.9 ± 1.2 a |
KB100 | 14.4 ± 2.4 a | 133.3 ± 13.6 bc | 58.8 ± 0.6 cd | 101.8 ± 6.1 b | 11.5 ± 0. 7 a |
KB75 | 11.8 ± 0.4 a | 152.8 ± 7.2 ab | 56.2 ± 0.2 d | 112.2 ± 7.1 b | 11.0 ± 0.7 a |
KB50 | 13.1 ± 2.2 a | 164.6 ± 9.8 a | 79.8 ± 0.5 a | 142.2 ± 4.7 a | 11.5 ± 1.4 a |
KB0 | 12.8 ± 2.5 a | 176.9 ± 4.9 a | 65.2 ± 0.9 b | 104.8 ±5.3 b | 11.3 ± 0.8 a |
Yield | Diameter | |||||
---|---|---|---|---|---|---|
Treatment 1 | Fruit Yield per Plant (g/plant) | Number of Fruits per Plant | Fruit Weight (g/fruit) | Yield Index | Polar (cm) | Equatorial (cm) |
KF100 | 270.1 ± 5.5 b | 14.5 ± 0.3 a | 18.6 ± 0.2 cd | 2.69± 0.04 b | 3.5 ± 0.28 a | 4.1 ± 0.34 a |
KF75 | 276.7 ± 4.5 ab | 13.0 ± 0.4 abc | 21.5 ± 0.8 a | 2.75 ± 0.03 ab | 3.7 ± 0.22 a | 4.5 ± 0.11 a |
KF50 | 279.1 ± 11.5 ab | 13.5 ± 1.2 ab | 20.6 ± 1.1 ab | 2.73 ± 0.07 ab | 3.5 ± 0.20 a | 4.4 ± 0.17 a |
KF0 | 215.3 ± 5.6 c | 12.2 ± 0.5 bc | 17.6 ± 0. 5 d | 2.31 ± 0.04 c | 3.3 ± 0.13 a | 4.1 ± 0.14 a |
KB100 | 229.0 ± 7.1 c | 11.6 ± 0. 7 c | 19.8 ± 0. 6 abc | 2.41 ± 0.04 c | 3.5 ± 0.27 a | 4.3 ± 0.22 a |
KB75 | 296.5 ± 8.6 a | 14.2 ± 0.4 a | 20.9 ± 0.1ab | 2.86 ± 0.06 a | 3.4 ± 0.15 a | 4.3 ± 0.30 a |
KB50 | 230.2 ± 10.9 c | 11.9 ± 0.4 bc | 19.3 ± 0.3 bcd | 2.42 ± 0.07 c | 3.4 ± 0.27 a | 4.3 ± 0.17 a |
KB0 | 287.2 ± 9.4 ab | 14.6 ± 0.4 a | 19.8 ± 1.1 abc | 2.80 ± 0.06 ab | 3.5 ± 0.02 a | 4.3 ± 0.39 a |
Treatment 1 | Total Soluble Solids (°Brix) | Titratable Acidity (%) | pH | Maturity Index | Ash (%) | Protein (%) | Fiber (%) | Moisture (%) | Fat (%) | Electric Conductivity (dS/m) |
---|---|---|---|---|---|---|---|---|---|---|
KF100 | 6.0 ± 0.01 ab | 0.83 ± 0.01 b | 3.90 ± 0.006 c | 7.3 ± 0.13 d | 0.64 ± 0.03 a | 1.1 ± 0.11 bc | 1.7 ± 0.07 abc | 91.3 ± 0.40 c | 0.76 ± 0.03 ab | 2.56 ± 0.11 a |
KF75 | 6.1 ± 0.06 a | 0.68 ± 0.01 c | 3.94 ± 0.006 b | 9.0 ± 0.10 b | 0.51 ± 0.03 b | 2.0 ± 0.21 a | 1.2 ± 0.21 cd | 91.7 ± 0.32 abc | 0.85 ± 0.06 a | 2.81 ± 0.72 a |
KF50 | 5.9 ± 0.06 b | 0.59 ± 0.01 d | 4.07 ± 0.006 a | 9.9 ± 0.06 a | 0.56 ± 0.03 ab | 1.1 ± 0.06 bc | 1.0 ± 0.06 d | 92.4 ± 0.51 a | 0.86 ± 0.01 a | 3.29 ± 0.10 a |
KF0 | 5.9 ± 0.01 ab | 0.94 ± 0.01 a | 3.82 ± 0.006 e | 6.3 ± 0.03 e | 0.53 ± 0.03 ab | 1.4 ± 0.33 ab | 1.8 ± 0.09 ab | 92.4 ± 0.34 ab | 0.58 ± 0.09 bc | 2.61 ± 0.13 a |
KB100 | 6.0 ± 0.01 ab | 0.60 ± 0.01 d | 3.89 ± 0.006 c | 10.0 ± 007 a | 0.63 ± 0.03 a | 1.8 ± 0.25 a | 1.9 ± 0.15 a | 91.9 ± 0.15 abc | 0.76 ± 0.04 ab | 2.52 ± 0.01 a |
KB75 | 5.8 ± 0.01 bc | 0.93 ± 0.01 a | 3.84 ± 0.001 d | 6.2 ± 0.05 e | 0.53 ± 0.06 ab | 1.7 ± 0.21 a | 1.3 ± 0.30 bcd | 92.4 ± 0.16 a | 0.81 ± 0.01 a | 3.14 ± 0.59 a |
KB50 | 5.6 ± 0.10 cd | 0.61 ± 0.01 d | 3.85 ± 0.001 d | 9.3 ± 0.27 b | 0.63 ± 0.04 a | 0.8 ± 0.28 c | 2.1 ± 0.33 a | 91.8 ± 0.31 abc | 0.52 ± 0.13 c | 3.48 ± 0.71 a |
KB0 | 5.5 ± 0.23 d | 0.70 ± 0.01 c | 3.96 ± 0.006 b | 7.8 ± 0.27 c | 0.63 ± 0.54 a | 0.6 ± 0.19 c | 2.1 ± 0.03 a | 91.5 ± 0.10 bc | 0.38 ± 0.10 c | 2.64 ± 0.06 a |
RT (min) | m/z (Da) | FC KB75/KF75 | p. Value | Name | Adduct | Mass Error (ppm) |
---|---|---|---|---|---|---|
4.29 | 683.2535 | 15.361 | 0.001397 | 4,4″-bis(N-feruloyl)serotonin | [M-H2O-H]− | 4 |
0.5 | 555.1149 | 8.0253 | 0.000612 | Salvianolic acid K | [M-H]− | 1 |
0.45 | 241.011 | 0.46791 | 0.009537 | Glucose 6-phosphate | [M-H2O-H]− | 1 |
1.37 | 111.008 | 0.43534 | 0.011994 | Citraconic acid | [M-H2O-H]− | 2 |
0.63 | 173.0085 | 0.43303 | 0.033027 | Citric acid | [M-H]− | 1 |
0.54 | 170.045 | 0.43188 | 0.008629 | N-Acetylglutamic acid | [M-H2O-H]− | 2 |
0.67 | 85.0286 | 0.39807 | 0.017379 | 2-Hydroxybutyric acid | [M-H2O-H]− | 4 |
0.48 | 146.0455 | 0.3797 | 0.000548 | L-Glutamic acid | [M-H]− | 3 |
0.45 | 132.0298 | 0.30059 | 0.000237 | L-Aspartic acid | [M-H]− | 3 |
3.15 | 205.0495 | 0.18011 | 2.41 × 10−7 | Sinapic acid | [M-H2O-H]− | 3 |
0.55 | 126.0552 | 0.17595 | 1.05 × 10−6 | 4-Acetamidobutanoic acid | [M-H2O-H]− | 2 |
1.83 | 323.0968 | 0.17585 | 1.47 × 10−7 | Sucrose | [M-H2O-H]− | 3 |
4.2 | 609.1436 | 0.17318 | 3.20 × 10−6 | Quercetin 3-O-rhamnoside 7-O-glucoside | [M-H]− | 4 |
3.72 | 565.2117 | 0.17204 | 4.39 × 10−7 | Magnesium protoporphyrin | [M-H2O-H]− | 4 |
3.08 | 193.0498 | 0.16864 | 8.50 × 10−6 | trans-Ferulic acid | [M-H]− | 4 |
2.27 | 203.0825 | 0.15452 | 6.88 × 10−6 | L-Tryptophan | [M-H]− | 1 |
12.07 | 293.2106 | 0.15073 | 5.64 × 10−6 | 13-L-Hydroperoxylinoleic acid | [M-H2O-H]− | 4 |
1.38 | 87.0085 | 0.14848 | 2.30 × 10−5 | Pyruvic acid | [M-H]− | 3 |
0.49 | 473.1517 | 0.14377 | 1.33 × 10−5 | alpha-D-Xylopyranosyl-(1->6)-beta-D-glucopyranosyl-(1->4)-D-glucose | [M-H]− | 1 |
0.85 | 515.1246 | 0.1309 | 6.55 × 10−5 | b-D-Glucuronopyranosyl-(1->3)-a-D-galacturonopyranosyl-(1->2)-L-rhamnose | [M-H]− | 2 |
13.88 | 393.1715 | 0.11576 | 0.000477 | 1,3,8-Trihydroxy-4-methyl-2,7-diprenylxanthone | [M-H]− | 2 |
Compound | Concentration (µg/g of Dried Sample) | |
---|---|---|
Non-Biofertilized (KF75) | Biofertilized (KB75) | |
Precursor | ||
Phenylalanine | 16.77 ± 0.60 a | 16.28 ± 0.09 a |
Phenolic acids | ||
t-Cinnamic acid | 0.89 ± 0.03 a | 0.15 ± 0.01 *b |
Ferulic acid | 2.62 ± 0.16a | 2.04 ± 0.04 b |
Protocatechuic acid | 0.17 ± 0.01 *a | 0.06 ± 0.005 *b |
Vanillic acid | 0.10 ± 0.01 *a | 0.11 ± 0.003 *a |
4-Coumaric acid | 0.64 ± 0.03 a | 0.44 ± 0.01 b |
Chlorogenic acid | 6.06 ± 0.13 a | 9.52 ± 0.12 b |
Sinapic acid | 1.44 ± 0.04 a | 0.93 ± 0.01 b |
Flavonoids | ||
Quercetin-3-glucoside | 0.79 ± 0.04 *a | 0.66 ± 0.01 *b |
Quercetin 3,4′-di-O-glucoside | 107.25 ± 7.34 a | 60.68 ± 2.21 b |
Rutin | 14.85 ± 0.85 a | 15.91 ± 0.21 a |
Number | Bacterial Inoculant | K Dose in Nutritive Solution | Treatment |
---|---|---|---|
T1 | No | 100% | KF100 |
T2 | 75% | KF75 | |
T3 | 50% | KF50 | |
T4 | 0% | KF0 | |
T5 | Yes | 100% | KB100 |
T6 | 75% | KB75 | |
T7 | 50% | KB50 | |
T8 | 0% | KB0 |
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Ramírez-Cariño, H.F.; Ochoa-Velasco, C.E.; Guerrero-Analco, J.A.; Monribot-Villanueva, J.L.; Calderón-García, C.; González-Terreros, E.; Escamirosa-Tinoco, C.; Morales, I.; Valadez-Blanco, R. Combined Effect of the Potassium Dose and Plant Biofertilization by Acinetobacter calcoaceticus on the Growth, Mineral Content, Nutritional Quality, Antioxidant Activity, and Metabolomic Features of Tomatillo Fruits (Physalis ixocarpa Brot.). Plants 2023, 12, 466. https://doi.org/10.3390/plants12030466
Ramírez-Cariño HF, Ochoa-Velasco CE, Guerrero-Analco JA, Monribot-Villanueva JL, Calderón-García C, González-Terreros E, Escamirosa-Tinoco C, Morales I, Valadez-Blanco R. Combined Effect of the Potassium Dose and Plant Biofertilization by Acinetobacter calcoaceticus on the Growth, Mineral Content, Nutritional Quality, Antioxidant Activity, and Metabolomic Features of Tomatillo Fruits (Physalis ixocarpa Brot.). Plants. 2023; 12(3):466. https://doi.org/10.3390/plants12030466
Chicago/Turabian StyleRamírez-Cariño, Heriberto F., Carlos E. Ochoa-Velasco, José A. Guerrero-Analco, Juan L. Monribot-Villanueva, Concepción Calderón-García, Elizabeth González-Terreros, Cirenio Escamirosa-Tinoco, Isidro Morales, and Rogelio Valadez-Blanco. 2023. "Combined Effect of the Potassium Dose and Plant Biofertilization by Acinetobacter calcoaceticus on the Growth, Mineral Content, Nutritional Quality, Antioxidant Activity, and Metabolomic Features of Tomatillo Fruits (Physalis ixocarpa Brot.)" Plants 12, no. 3: 466. https://doi.org/10.3390/plants12030466
APA StyleRamírez-Cariño, H. F., Ochoa-Velasco, C. E., Guerrero-Analco, J. A., Monribot-Villanueva, J. L., Calderón-García, C., González-Terreros, E., Escamirosa-Tinoco, C., Morales, I., & Valadez-Blanco, R. (2023). Combined Effect of the Potassium Dose and Plant Biofertilization by Acinetobacter calcoaceticus on the Growth, Mineral Content, Nutritional Quality, Antioxidant Activity, and Metabolomic Features of Tomatillo Fruits (Physalis ixocarpa Brot.). Plants, 12(3), 466. https://doi.org/10.3390/plants12030466