Effects of UV Stress in Promoting Antioxidant Activities in Fungal Species Тrametes versicolor (L.) Lloyd and Flammulina velutipes (Curtis) Singer
Abstract
:1. Introduction
2. Materials and Methods
2.1. Fungal Material
2.2. Submerged Cultivation and Preparation of Extracts
2.3. LC-MS/MS Quantification of Selected Phenolic Compounds
2.4. Determination of Total Phenolic (TP) and Total Protein (TPR) Contents
2.5. DPPH Radical Scavenging Assay
2.6. Hydroxyl Radical (OH•) Scavenging Assay
2.7. Superoxide Anion Radical Scavenging Assay (SOA)
2.8. Ferrous Ion Chelating Assay (FRAP)
2.9. Statistical Analysis
3. Results аnd Discussion
3.1. Mycelial Growth
3.2. Mycochemical Characterization
3.2.1. LC–MS/MS Analysis
3.2.2. Total Phenolic Content (TP)
3.2.3. Total Protein Content (TPR)
3.3. In Vitro AO Activity
3.3.1. DPPH Assay
3.3.2. SOA Assay
3.3.3. OH Assay
3.3.4. FRAP Assay
3.4. Correlation Analysis
3.5. Principal Component Analysis (PCA)
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Class of Analyzed Compounds | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|
Hydroxybenzoic Acid | Hydroxycinnamic Acid | Cyclohexanecarboxylic Acid | Isoflavonoid | Biflavonoid | Flavone | |||||
Analyzed Sample | Incubation Time (Days) | p-Hydroxybenzoic Acid | Protocatechuic Acid | Vanillic Acid | p-Coumaric Acid | Quinic Acid | Daidzein | Genistein | Amentoflavone | Apiin |
Flammulina velutipes | ||||||||||
F | 7 | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. |
14 | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | |
21 | 26,996.5 | 5405.0 | 18.0 | 8.0 | 63.5 | 642.0 | 440.5 | 0 | 0 | |
28 | 14,234.5 | 1759.5 | 70.0 | 6853.0 | 68.5 | 854.5 | 345.5 | 0 | 0 | |
Fcont. | 7 | 15,233.5 | 2261.0 | 17.0 | 75.5 | 63.5 | 1316.0 | 943.5 | 306 | 0 |
14 | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | |
21 | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | |
28 | 19,580.5 | 4501.5 | 107.5 | 327.5 | 30 | 641 | 390 | 0 | 0 | |
M | 7 | 11,102.0 | 970 | 0 | 107 | 158.5 | 1702.5 | 3210.5 | 1115.5 | 114 |
14 | 12,027.0 | 1475.5 | 21.5 | 106.5 | 81.5 | 1906.5 | 3152 | 0 | 266 | |
21 | 18,650,0 | 1555.0 | 56.5 | 52 | 72.5 | 1226 | 1966.5 | 0 | 85 | |
28 | 8900.0 | 3680.5 | 28 | 4756 | 43 | 1109.5 | 1304 | 0 | 89 | |
M cont. | 7 | 15,364.5 | 1475.5 | 21.5 | 102.5 | 204.5 | 2539 | 4824.0 | 0 | 1589 |
14 | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | |
21 | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | |
28 | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | |
Range | 8900–26,996.5 | 970–5405.0 | 17.0–107.5 | 8.0–6853.0 | 30–204.5 | 641–1906 | 345.5–4824.0 | 306–1115.5 | 85–1589 | |
Trametes versicolor | ||||||||||
F | 7 | 2081.0 | 19.5 | 0 | 36.5 | 341.5 | 189.5 | 148.5 | 0 | 0 |
14 | 365 | 29 | 0 | 0 | 147.5 | 9 | 12 | 0 | 0 | |
21 | 275.5 | 33.5 | 0 | 0 | 127 | 13.5 | 0 | 782 | 96.5 | |
28 | 417.5 | 13 | 0 | 0 | 85 | 0 | 0 | 1934.5 | 0 | |
F cont. | 7 | 984.5 | 18.5 | 0 | 0 | 440.5 | 8 | 19.5 | 0 | 0 |
14 | 275.5 | 36.5 | 0 | 0 | 84.5 | 5 | 2.5 | 404 | 0 | |
21 | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | |
28 | 45 | 0 | 0 | 0 | 53.5 | 0 | 0 | 0 | 0 | |
M | 7 | 172.5 | 5.5 | 0 | 21 | 82 | 0 | 0 | 0 | 56 |
14 | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | |
21 | 83 | 7 | 0 | 11 | 70 | 5 | 5 | 0 | 25 | |
28 | 1200 | 26 | 0 | 0 | 170.5 | 4 | 13.5 | 594.5 | 140.5 | |
M cont. | 7 | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. |
14 | 166 | 43.5 | 0 | 0 | 103 | 0 | 12 | 0 | 134.5 | |
21 | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | n.a. | |
28 | 262 | 11.5 | 29 | 0 | 48 | 5 | 35 | 0 | 104 | |
Range | 45–2081 | 5.5–43.5 | 0–29 | 11–36.5 | 48–440.5 | 4–189.5 | 5–148.5 | 404–1934.5 | 25–140.5 |
Extracts | TP (mg GAE/mg d.w.) | TPR (mg BSAE/g d.w.) | |||
---|---|---|---|---|---|
T. versicolor | UV exposed | Control | UV exposed | Control | |
F | 7 days | 49.28 ± 0.83 a,c | 43.74 ± 0.45 a,c | 102.90 ± 2.20 a,c | 103.93 ± 3.59 a,c |
14 days | 48.43 ± 0.13 a,c | 47.22 ± 0.49 a,c | 79.40 ± 0.40 a,c | 64.80 ± 3.64 a,c | |
21 days | 50.03 ± 0.66 a,c | 19.22 ± 0.22 a,c | 77.50 ± 1.50 a,c | 115.29 ± 1.11 a,c | |
28 days | 18.78 ± 0.37 a,c | 8.61 ± 0.14 a,c | 103.16 ± 1.55 a,c | 117.73 ± 2.83 a,c | |
M | 7 days | 47.36 ± 0.61 a,c | 12.67 ± 0.44 a,c | 122.98 ± 2.07 a,c | 74.33 ± 0.36 a,c |
14 days | 18.03 ± 0.39 a,c | 15.56 ± 0.30 a,c | 100.82 ± 0.50 a,c | 106.37 ± 3.27 a,c | |
21 days | 17.86 ± 0.40 a,c | 15.94 ± 0.15 a,c | 99.15 ± 2.60 a,c | 114.95 ± 3.27 a,c | |
28 days | 18.84 ± 0.35 a,c | 11.19 ± 0.33 a,c | 183.53 ± 2.84 a,c | 75.02 ± 0.86 a,c | |
F. velutipes | UV exposed | Control | UV exposed | Control | |
F | 7 days | 17.26 ± 0.26b,c | 17.81 ± 0.03 b,c | 112.90 ± 1.20 b,c | 103.93 ± 3.59 b,c |
14 days | 18.35 ± 0.33 b,c | 14.86 ± 0.55 b,c | 133.16 ± 1.45 b,c | 117.73 ± 2.83 b,c | |
21 days | 16.98 ± 0.15 b,c | 16.69 ± 0.39 b,c | 99.50 ± 1.40 b,c | 95.29 ± 1.11 b,c | |
28 days | 16.91 ± 0.11 b,c | 19.03 ± 0.39 b,c | 77.40 ± 0.0 b,c | 64.80 ± 3.64 b,c | |
M | 7 days | 54.24 ± 0.35 b,d | 24.95 ± 1.28 b,d | 98.65 ± 1.58 b,c | 15.60 ± 0.88 b,c |
14 days | 59.60 ± 0.14 b,d | 58.34 ± 1.70 b,d | 75.58 ± 0.36 b,c | 19.67 ± 1.39 b,c | |
21 days | 25.19 ± 2.65 b,d | 34.06 ± 0.96 b,d | 42.07 ± 2.25 b,c | 25.34 ± 0.17 b,c | |
28 days | 21.94 ± 0.23 b,d | 13.71 ± 0.14 b,d | 8.56 ± 0.45 b,c | 14.01 ± 0.56 b,c |
Extracts | DPPH (%) | OH (%) | SOA (%) | FRAP (mg AAE/g d.w.) | |||||
---|---|---|---|---|---|---|---|---|---|
T. versicolor | |||||||||
UV exposed | Control | UV exposed | Control | UV exposed | Control | UV exposed | Control | ||
F | 7 days | 8.20 ± 0.11 a,c,e | 7.48 ± 0.22 a,c,e | 36.34 ± 2.45 a,c,e | 23.93 ± 0.60 a,d,e | 72.53 ± 0.38 a,c,e | 73.07 ± 2.23 a,c,e | 15.80 ± 0.21 a,c,e | 16.87 ± 0.20 a,c,e |
14 days | 8.21 ± 0.12 a,c,e | 7.95 ± 0.06 a,c,e | 24.65 ± 0.46 a,c,e | 26.79 ± 1.92 a,d,e | 73.55 ± 1.81 a,c,e | 71.90 ± 1.55 a,c,e | 15.43 ± 0.28 a,c,e | 15.55 ± 0.30 a,c,e | |
21 days | 7.94 ± 0.09 a,c,e | 7.99 ± 0.15 a,c,e | 15.68 ± 2.00 a,c,e | 24.69 ± 0.19 a,d,e | 73.34 ± 1.14 a,c,e | 34.35 ± 0.52 a,c,e | 15.44 ± 0.42 a,c,e | 18.63 ± 1.30 a,c,e | |
28 days | 7.88 ± 0.31 a,c,e | 3.96 ± 0.73 a,c,e | 36.36 ± 1.06 a,c,e | N.A. | 66.00 ± 0.48 a,c,e | 70.58 ± 0.10 a,c,e | 17.76 ± 0.01 a,c,e | 5.05 ± 0.27 a,c,e | |
M | 7 days | 8.22 ± 0.41 a,c,e | 6.97 ± 0.14 a,c,e | 30.33 ± 1.15 a,c,e | 29.16 ± 1.91 a,c,e | 44.83 ± 1.24 a,c,e | 72.74 ± 0.10 a,c,e | 19.88 ± 0.34 a,c,e | 9.95 ± 0.21 a,c,e |
14 days | 8.36 ± 0.08 a,c,e | 8.70 ± 0.08 a,c,e | 30.88 ± 3.84 a,c,e | 4.98 ± 0.31 a,c,e | 69.43 ± 0.57 a,c,e | 58.45 ± 1.43 a,c,e | 24.11 ± 0.59 a,c,e | 22.85 ± 0.50 a,c,e | |
21 days | 8.86 ± 0.13 a,c,e | 8.05 ± 0.47 a,c,e | 32.22 ± 1.98 a,c,e | 39.19 ± 2.96 a,c,e | 70.92 ± 1.72 a,c,e | 55.82 ± 2.10 a,c,e | 22.90 ± 0.40 a,c,e | 21.25 ± 0.90 a,c,e | |
28 days | 8.56 ± 0.22 a,c,e | 4.29 ± 0.07 a,c,e | 51.78 ± 0.61 a,c,e | 22.82 ± 1.67 a,c,e | 57.57 ± 0.95 a,c,e | 68.15 ± 0.86 a,c,e | 26.79 ± 0.33 a,c,e | 24.89 ± 0.25 a,c,e | |
F. velutipes | |||||||||
UV exposed | Control | UV exposed | Control | UV exposed | Control | UV exposed | Control | ||
F | 7 days | 3.13 ± 0.52 b,c,e | 1.17 ± 0.18 b,c,e | 23.15 ± 1.57 a,c,e | 16.61 ± 1.96 a,c,e | 68.99 ± 0.70 b,c,e | 29.44 ± 0.30 b,c,e | 74.62 ± 0.09 b,c,e | 78.25 ± 1.10 b,c,e |
14 days | 4.53 ± 0.29 b,c,e | 3.10 ± 0.33 b,c,e | 24.55 ± 1.70 a,c,e | 8.04 ± 1.48 a,c,e | 68.06 ± 0.01 b,c,e | 25.46 ± 0.33 b,c,e | 85.36 ± 0.50 b,c,e | 23.72 ± 0.61 b,c,e | |
21 days | 7.08 ± 0.58 b,c,e | 4.04 ± 0.05 b,c,e | 51.46 ± 0.02 a,c,e | 15.67 ± 2.11 a,c,e | 71.29 ± 0.54 b,c,e | 71.12 ± 0.31 b,c,e | 74.66 ± 0.23 b,c,e | 64.71 ± 1.74 b,c,e | |
28 days | 5.25 ± 0.05 b,c,e | 7.26 ± 0.27 b,c,e | 30.58 ± 4.84 a,c,e | 25.40 ± 1.64 a,c,e | 71.16 ± 0.93 b,c,e | 71.45 ± 0.31 b,c,e | 56.08 ± 0.53 b,c,e | 83.10 ± 2.72 b,c,e | |
M | 7 days | 6.23 ± 0.19 b,c,e | 7.00 ± 0.12 b,c,e | 26.10 ± 2.96 a,c,e | N.D. | 48.04 ± 1.70 b,c,f | 59.74 ± 2.79 b,c,f | 55.87 ± 0.36 b,c,f | 32.12 ± 1.65 b,c,f |
14 days | 7.04 ± 0.12 b,c,e | 2.90 ± 0.02 b,c,e | 12.53 ± 1.52 a,c,e | N.D. | 34.69 ± 2.01 b,c,f | 23.96 ± 1.39 b,c,f | 61.39 ± 0.14 b,c,f | 60.09 ± 1.75 b,c,f | |
21 days | 6.60 ± 0.62 b,c,e | 8.14 ± 0.10 b,c,e | 42.68 ± 2.17 a,c,e | 39.96 ± 2.14 a,c,e | 37.75 ± 0.93 b,c,f | 40.21 ± 2.24 b,c,f | 25.94 ± 2.73 b,c,f | 35.08 ± 0.99 b,c,f | |
28 days | 8.00 ± 0.05 b,c,e | 7.68 ± 0.32 b,c,e | 49.49 ± 2.62 a,c,e | N.D. | 41.36 ± 0.31 b,c,f | 21.12 ± 0.71 b,c,f | N.A. | N.A. |
Correlation Coefficient—R2 | |||||||||
---|---|---|---|---|---|---|---|---|---|
Extracts | DPPH/TP | OH/TP | SOA/TP | FRAP/TP | |||||
T. versicolor | |||||||||
UV exposed | Control | UV exposed | Control | UV exposed | Control | UV exposed | Control | ||
F | 7 days | 0.01 | 0.58 * | 0.01 | 0.03 | 0.01 | 0.53 * | 0.13 | 0.22 |
14 days | 0.73 * | 0.45 | 0.63 * | 0.23 | 0.61 * | 0.26 | 0.91 * | 0.08 | |
21 days | 0.97 * | 0.35 | 0.08 | 0.85 * | 0.33 | 0.86 * | 0.87 * | 0.03 | |
28 days | 0.01 | 0.48 | 0.44 | / | 0.44 | 1.00 | 0.05 | 0.21 | |
M | 7 days | 0.99 * | 0.70 * | 0.83 * | 0.93 * | 0.73 * | 0.08 | 0.88 * | 0.09 |
14 days | 0.97 * | 0.42 | 0.01 | 0.64 * | 0.85 * | 0.85 * | 0.40 | 0.89 * | |
21 days | 0.74 * | 0.36 | 0.76 * | 0.42 | 0.02 | 0.97 | 0.16 | 1.00 * | |
28 days | 0.21 | 0.65* | 0.40 | 0.99 * | 0.40 | 0.16 | 0.01 | 0.82 * | |
F. velutipes | |||||||||
UV exposed | Control | UV exposed | Control | UV exposed | Control | UV exposed | Control | ||
F | 7 days | 0.36 | 0.73 * | 0.36 | 0.07 | 0.36 | 0.01 | 0.01 | 0.56 * |
14 days | 0.04 | 0.54 * | 0.56 * | 0.91 * | 0.10 | 0.18 | 0.02 | 0.04 | |
21 days | 0.81 * | 0.30 | 0.98 * | 0.27 | 0.68 * | 1.00 * | 0.98 * | 0.45 | |
28 days | 0.01 | 0.22 | 0.01 | 0.08 | 0.01 | 0.48 | 0.96 * | 0.59 * | |
M | 7 days | 0.55 * | 0.93 * | 0.67 * | / | 0.01 | 0.99 * | 1.00 * | 0.16 |
14 days | 0.97 * | 0.83 * | 0.01 | / | 0.65 * | 0.03 | 1.00 * | 0.03 | |
21 days | 0.12 | 0.47 | 0.40 | 0.43 | 0.12 | 0.88 * | 1.00 * | 1.00 * | |
28 days | 0.07 | 0.98 * | 0.84 * | / | 0.64 * | 0.64 * | / | / |
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Krsmanović, N.; Rašeta, M.; Mišković, J.; Bekvalac, K.; Bogavac, M.; Karaman, M.; Isikhuemhen, O.S. Effects of UV Stress in Promoting Antioxidant Activities in Fungal Species Тrametes versicolor (L.) Lloyd and Flammulina velutipes (Curtis) Singer. Antioxidants 2023, 12, 302. https://doi.org/10.3390/antiox12020302
Krsmanović N, Rašeta M, Mišković J, Bekvalac K, Bogavac M, Karaman M, Isikhuemhen OS. Effects of UV Stress in Promoting Antioxidant Activities in Fungal Species Тrametes versicolor (L.) Lloyd and Flammulina velutipes (Curtis) Singer. Antioxidants. 2023; 12(2):302. https://doi.org/10.3390/antiox12020302
Chicago/Turabian StyleKrsmanović, Nenad, Milena Rašeta, Jovana Mišković, Kristina Bekvalac, Mirjana Bogavac, Maja Karaman, and Omoanghe S. Isikhuemhen. 2023. "Effects of UV Stress in Promoting Antioxidant Activities in Fungal Species Тrametes versicolor (L.) Lloyd and Flammulina velutipes (Curtis) Singer" Antioxidants 12, no. 2: 302. https://doi.org/10.3390/antiox12020302