Influence on Secondary Metabolism of Piper nigrum L. by Co-Inoculation with Arbuscular Mycorrhizal Fungi and Fusarium solani f. sp. piperis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Material
2.2. Preparation of Arbuscular Mycorrhizal Fungal Spore Inoculum and Inoculation
2.3. Acquisition, Isolation, and Culture of Fusarium solani f. sp. piperis Phytopathogen
2.4. Experimental Design and Material Collection
2.5. Inoculation, Observation of Symptoms and Recovery of Fusarium solani f. sp. piperis
2.6. Extraction and Volatile Compounds
2.7. Lipoxygenase (LOX) Activity
2.8. Phenylalanine Ammonia Lyase (PAL) Activity
2.9. Total Phenolics Determination
2.10. Statistical Analyses
3. Results
3.1. Aspects of Infection
3.2. Oil Essential Composition
3.3. Total Phenolic Content
3.4. Enzymatic Activity
3.4.1. Lipoxygenase Enzyme
3.4.2. Phenylalanine Ammonia-Lyase Enzymatic Activity
3.5. Hierarchical Cluster Analysis
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Compounds | RIa | RIb | 7 dpi | 21 dpi | ||||
---|---|---|---|---|---|---|---|---|
CONTROL | FUS | AMF + FUS | CONTROL | FUS | AMF + FUS | |||
2E-hexenal | 846 | 846 | 17.98 ± 5.20 A | 6.11 ± 3.77 B | 1.16 ± 0.92 B | 2.21 ± 0.58 C | 3.50 ± 1.68 C | 3.06 ± 0.83 C |
δ-elemene | 1335 | 1339 | 2.92 ± 0.14 | 5.20 ± 0.34 | 5.15 ± 0.82 | 4.11 ± 0.18 | 4.02 ± 0.66 | 3.42 ± 0.11 |
α-cubebene | 1345 | 1352 | 2.70 ± 0.19 | 4.17 ± 0.77 | 3.42 ± 0.30 | 2.45 ± 0.32 | 2.86 ± 0.14 | 2.87 ± 0.09 |
α-copaene | 1374 | 1378 | 1.95 ± 0.45 | 6.32 ± 2.68 | 6.16 ± 0.90 | 4.11 ± 0.39 | 3.67 ± 0.34 | 4.46 ± 0.22 |
β-cubebene | 1387 | 1392 | 3.32 ± 0.55 | 2.93 ± 0.81 | 0.0 | 1.08 ± 0.06 | 0.89 ± 0.03 | 1.10 ± 0.13 |
α-gurjunene | 1409 | 1413 | 0.97 ± 0.23 | 4.78 ± 2.43 | 3.94 ± 0.20 | 3.46 ± 0.14 | 3.89 ± 0.32 | 3.62 ± 0.09 |
β-caryophyllene | 1417 | 1423 | 2.76 ± 0.63 | 5.32 ± 1.15 | 4.73 ± 0.23 | 4.07 ± 0.33 | 6.54 ± 1.78 | 3.80 ± 0.27 |
β-selinene | 1489 | 1491 | 1.94 ± 0.49 | 5.26 ± 0.89 | 3.86 ± 0.48 | 4.40 ± 0.28 | 4.36 ± 0.42 | 3.57 ± 0.16 |
Z-β-guaiene | 1492 | 1500 | 0.0 | 0.0 | 0.0 | 6.59 | 0.0 | 0.0 |
viridiflorene | 1496 | 1500 | 5.36 ± 0.13 | 5.78 ± 0.88 | 0.0 | 0.0 | 0.0 | 0.0 |
bicyclogermacrene | 1500 | 1502 | 4.60 ± 0.48 | 4.12 ± 3.15 | 11.82 ± 4.75 | 5.20 ± 0.28 | 4.21 ± 0.79 | 7.13 ± 2.17 |
α-muurolene | 1500 | 1505 | 1.63 ± 0.32 A | 2.49 ± 0.63 A | 3.31 ± 0.62 A | 16.68 ± 2.44 B | 0.0 C | 3.08 ± 0.18 D |
E-β-guaiene | 1502 | 1522 | 0.0 | 4.77 ± 0.84 | 0.0 | 0.0 | 0.0 | 0.0 |
δ-amorphene | 1511 | 1512 | 0.0 | 2.18 ± 1.93 | 0.0 | 0.0 | 0.0 | 0.52 ± 0.12 |
γ-cadinene | 1513 | 1521 | 6.78 ± 0.70 | 8.82 ± 0.40 | 0.0 | 0.0 | 0.0 | 5.45 ± 0.14 |
δ-cadinene | 1513 | 1522 | 3.630.57 | 3.92 ± 0.39 | 4.16 ± 0.87 | 10.60 ± 0.57 | 10.07 ± 0.55 | 5.23 ± 0.69 |
E-nerolidol | 1561 | 1567 | 2.42 ± 0.70 | 1.11 ± 0.56 | 1.94 ± 0.79 | 2.96 ± 0.62 | 2.08 ± 0.28 | 1.04 ± 0.12 |
caryophyllene oxide | 1582 | 1589 | 1.33 ± 0.29 | 1.02 ± 0.23 | 1.50 ± 0.09 | 2.03 ± 0.26 | 1.38 ± 0.17 | 1.52 ± 0.33 |
α-epi-muurolol | 1640 | 1647 | 3.05 ± 0.84 | 3.97 ± 0.78 | 0.0 | 0.0 | 0.0 | 0.0 |
α-muurolol | 1644 | 1651 | 20.59 ± 2.71 A | 24.52 ± 0.83 B | 0.0 C | 0.0 D | 3.23 ± 0.27 E | 10.91 ± 0.44 F |
cubenol | 1645 | 1653 | 0.0 | 14.20 ± 4.73 | 18.97 ± 2.02 | 3.15 ± 0.08 | 9.07 ± 0.34 | 1.79 |
α-cadinol | 1652 | 1659 | 0.86 ± 0.29 | 1.44 ± 0.47 | 0.56 ± 0.06 | 0.0 | 0.0 | 4.39 ± 0.36 |
Monoterpene hydrocarbons | 0.27 ± 0.43 | 0.0 | 0.0 | 0.76 ± 0.09 | 1.90 ± 0.51 | 3.64 ± 2.12 | ||
Oxygenated monoterpenes | 0.72 ± 0.20 | 1.05 ± 0.58 | 0.0 | 1.40 ± 0.22 | 1.49 ± 0.24 | 1.59 ± 0.31 | ||
Sesquiterpene hydrocarbons | 45.09 ± 7.54 A | 78.86 ± 20.67 A | 56.25 ± 10.41 A | 72.92 ± 6.86 A | 51.93 ± 6.80 A | 55.20 ± 6.40 A | ||
Oxygenated Sesquiterpenes | 29.96 ± 5.70 A | 50.04 ± 9.39 A,B | 28.64 ± 4.64 A,C | 15.35 ± 2.90 A | 21.69 ± 2.98 A | 24.63 ± 3.82 A | ||
Phenylpropanoids | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | ||
Others | 18.36 ± 5.40 | 6.29 ± 3.83 | 2.48 ± 1.18 | 3.24 ± 1.15 | 4.97 ± 2.01 | 5.09 ± 1.94 | ||
Total | 94.40 ± 19.27 | 136.25 ± 34.48 | 87.37 ± 16.23 | 93.67 ± 11.21 | 81.98 ± 12.53 | 90.15 ± 14.58 |
Compounds | RIa | RIb | 7 dpi | 21 dpi | ||||
---|---|---|---|---|---|---|---|---|
CONTROL | FUS | AMF + FUS | CONTROL | FUS | AMF + FUS | |||
n-octane | 800 | 775 | 0.0 | 0.0 | 7.72 ± 3.30 | 0.0 | 0.0 | 0.0 |
n-nonane | 900 | 900 | 3.53 ± 0.84 | 4.02 ± 0.47 | 3.79 ± 1.61 | 4.70 ± 0.71 | 8.24 ± 1.25 | 7.23 ± 0.95 |
α-pinene | 932 | 927 | 2.28 ± 0.41 | 2.76 ± 0.24 | 1.75 ± 0.26 | 3.42 ± 0.76 | 3.58 ± 0.43 | 3.44 ± 1.07 |
canfene | 946 | 945 | 1.64 ± 0.93 | 3.95 ± 1.30 | 1.46 ± 0.53 | 8.17 ± 0.34 | 6.36 ± 1.25 | 4.50 ± 1.95 |
β-pinene | 974 | 971 | 4.05 ± 1.38 | 3.11 ± 0.46 | 2.16 ± 0.20 | 3.42 ± 1.10 | 3.98 ± 0.76 | 3.71 ± 1.57 |
limonene | 1024 | 1022 | 6.31 ± 1.70 | 4.88 ± 0.69 | 3.44 ± 0.30 | 6.25 ± 1.49 | 5.81 ± 1.64 | 6.53 ± 2.12 |
camphor | 1141 | 1146 | 1.82 ± 0.49 | 3.17 ± 0.56 | 0.87 ± 0.46 | 1.57 ± 0.38 | 1.36 ± 0.59 | 0.46 ± 0.14 |
isoborneol | 1155 | 1158 | 1.62 ± 0.45 | 0.54 ± 0.13 | 0.44 ± 0.19 | 2.31 ± 0.36 | 1.60 ± 0.35 | 0.62 ± 0.10 |
δ-elemene | 1335 | 1337 | 12.68 ± 1.23 | 8.90 ± 1.88 | 10.33 ± 3.50 | 4.06 ± 2.41 | 5.50 ± 2.46 | 2.98 ± 0.92 |
β-caryophyllene | 1417 | 1423 | 32.93 ± 5.34 | 34.58 ± 2.38 | 42.79 ± 9.36 | 26.60 ± 3.21 | 27.21 ± 1.80 | 26.32 ± 1.16 |
Monoterpene hydrocarbons | 15.37 ± 4.86 | 15.74 ± 3.17 | 15.37 ± 4.86 | 22.63 ± 4.19 | 21.10 ± 4.37 | 19.75 ± 7.13 | ||
Oxygenated monoterpenes | 3.44 ± 0.95 | 3.71 ± 0.68 | 1.31 ± 0.65 | 3.88 ± 0.74 A,B | 2.96 ± 0.93 A | 1.08 ± 0.24 A,C | ||
Sesquiterpene hydrocarbons | 51.80 ± 7.81 | 49.61 ± 5.34 | 51.80 ± 7.81 | 35.37 ± 7.23 | 37.07 ± 5.67 | 32.91 ± 3.06 | ||
Oxygenated Sesquiterpenes | 2.18 ± 0.84 | 3.48 ± 0.83 | 2.42 ± 0.18 | 2.42 ± 1.12 | 0.20 ± 0.04 | 0.94 ± 0.60 | ||
Others | 3.66 ± 0.91 | 4.19 ± 0.49 | 11.62 ± 4.91 | 5.68 ± 0.84 | 8.70 ± 1.29 | 7.61 ± 0.99 | ||
Total | 76.44 ± 15.37 | 76.74 ± 10.51 | 76.44 ± 15.37 | 69.98 ± 14.11 | 70.03 ± 12.30 | 62.29 ± 12.02 |
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Trindade, R.; Almeida, L.; Xavier, L.; Andrade, E.H.; Maia, J.G.; Mello, A.; Setzer, W.N.; Ramos, A.; da Silva, J.K.R. Influence on Secondary Metabolism of Piper nigrum L. by Co-Inoculation with Arbuscular Mycorrhizal Fungi and Fusarium solani f. sp. piperis. Microorganisms 2021, 9, 484. https://doi.org/10.3390/microorganisms9030484
Trindade R, Almeida L, Xavier L, Andrade EH, Maia JG, Mello A, Setzer WN, Ramos A, da Silva JKR. Influence on Secondary Metabolism of Piper nigrum L. by Co-Inoculation with Arbuscular Mycorrhizal Fungi and Fusarium solani f. sp. piperis. Microorganisms. 2021; 9(3):484. https://doi.org/10.3390/microorganisms9030484
Chicago/Turabian StyleTrindade, Rafaela, Laís Almeida, Luciana Xavier, Eloisa Helena Andrade, José Guilherme Maia, Andréa Mello, William N. Setzer, Alessandra Ramos, and Joyce Kelly R. da Silva. 2021. "Influence on Secondary Metabolism of Piper nigrum L. by Co-Inoculation with Arbuscular Mycorrhizal Fungi and Fusarium solani f. sp. piperis" Microorganisms 9, no. 3: 484. https://doi.org/10.3390/microorganisms9030484