Improved Mineral Acquisition, Sugars Metabolism and Redox Status after Mycorrhizal Inoculation Are the Basis for Tolerance to Vanadium Stress in C3 and C4 Grasses
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Materials and Growth Conditions
2.2. Colonization and AMF Growth Analysis
2.3. Determination of Minerals Content
2.4. Photosynthetic Rate
2.5. Root Phosphatase Activities, Citrate and Proline Content
2.6. Extraction and Assessment of Sugars and Their Key Metabolizing Enzymes
2.7. Quantification of Detoxification-Related Parameters
2.8. Quantification of Total Vanadium
2.9. Lipid Peroxidation Determination
2.10. H2O2 Concentration Quantification
2.11. Total Antioxidant Capacity
2.12. Ascorbate, Glutathione, and Their Redox Status
2.13. Tocopherols
2.14. Polyphenols and Flavonoids
2.15. Enzyme Assays
2.15.1. Photorespiration Enzymes
2.15.2. Oxidative Stress-Related Enzymes
2.15.3. Antioxidant Enzymes
2.16. Ascorbate Biosynthesis Enzymes
2.16.1. L-Galactono-1,4-Lactone Dehydrogenase (GalLDH) Activity
2.16.2. D-Galacturonic Acid Reductase (GalUR) Activity
2.17. Statistical Analysis, Heat Map, Principal Component Analyses (PCA) and % of Change
3. Results
3.1. Soil Analysis
3.2. Root Colonization and Content of Phosphatases, Proline and Citrate
3.3. Minerals Content in Roots and Shoots
3.4. Vanadium Accumulation
3.5. Growth
3.6. Photosynthesis
3.7. The Sugars Metabolism
3.8. Oxidative Stress and Photorespiration
3.9. Heavy Metals Chelating Proteins
3.10. Nonenzymatic Antioxidants
3.11. Enzymatic Antioxidants
3.12. Ascorbate Biosynthesis
3.13. Principal Components Analysis
4. Discussion
5. Conclusions
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 | V Content | Phenolic Content | Citrate Content | Alkaline Phosphatase | Acid Phosphatase | Proline Content | Citrate Content | Mycorrhizal Colonization (%) | Hyphal Length (cm.g-1 Soil) | No. Arbuscules (No. cm-1 Root) | |
---|---|---|---|---|---|---|---|---|---|---|---|
Rye | Control | nd | 74.8 ± 0.8 b | 10.9 ± 1.2 a | 3.1 ± 0.3 a,b | 5.6 ± 0.1 b | 4.3 ± 0.8 a | 2.4 ± 0.17 a | 0 ± 0 a | 0 ± 0 a | 0 ± 0 a |
Myco | nd | 118 ± 15 a | 6.94 ± 0.2 a | 5.5 ± 0.7 d | 8 ± 0.9 c | 7.6 ± 0.1 c | 4.8 ± 0.31 b | 55.3 ± 3.7 c | 18.3 ± 0.9 c | 4.4 ± 0.01 b | |
V | 77 ± 1.3 b | 101.9 ± 3 a | 7.05 ± 0.6 a | 2.4 ± 0.4 a | 3.5 ± 0.5 a | 4.7 ± 0.5 a | 3.1 ± 0.22 a | 0 ± 0 a | 0 ± 0 a | 0 ± 0 a | |
Myco + V | 98 ± 5.4 a | 145 ± 28 a | 11.8 ± 1.6 a | 3.9 ± 0.2 c | 5.6 ± 0.7 b | 5.8 ± 0.9 b | 5.8 ± 0.26 b | 30.3 ± 1.8 b | 10.8 ± 1.75 b | 3.2 ± 0.83 b | |
Sorghium | Control | nd | 75.12 ± 9 b | 2.76 ± 0.1 c | 4 ± 0.53 a | 7.5 ± 0.4 b | 6.6 ± 0.4 a | 2.4 ± 0.16 a | 0 ± 0 a | 0 ± 0 a | 0 ± 0 a |
Myco | nd | 79 ± 7 b | 6.19 ± 0.7 b | 8.9 ± 0.1 b | 9.6 ± 0.5 b | 9.7 ± 0.7 b | 5.4 ± 0.3 c | 60 ± 2.6 c | 24.9 ± 0.5 c | 6.1 ± 0.5 c | |
V | 77 ± 5.2 a | 149 ± 10 a | 7.12 ± 0.5 b | 3 ± 0.66 a | 5.1 ± 0.5 a | 6 ± 0.5 a | 3.6 ± 0.24 b | 0 ± 0 a | 0 ± 0 a | 0 ± 0 a | |
Myco + V | 108 ± 7 b | 186 ± 13 a | 15.38 ± 1 a | 4.9 ± 0.4 a | 8.3 ± 0.2 b | 8.1 ± 0.3 b | 7.7 ± 0.14 d | 47.9 ± 2.7 b | 19.3 ± 1.4 b | 4.9 ± 0.6 b |
Organ | Treatment | K | Ca | Mg | P | Mn | Zn | |
---|---|---|---|---|---|---|---|---|
Rye | Shoot | Control | 2.38 ± 0.13 b | 0.50 ± 0.02 a | 0.55 ± 0.02 a | 3.46 ± 0.21 a,b | 0.18 ± 0.01 a,b | 0.07 ± 0.002 a |
Myco | 3.03 ± 0.25 a | 0.46 ± 0.04 a | 0.47 ± 0.04 a,b | 4.10 ± 0.34 a | 0.20 ± 0.02 a | 0.04 ± 0.003 a | ||
V | 0.67 ± 0.09 c | 0.34 ± 0.02 b | 0.41 ± 0.02 b | 1.30 ± 0.11 c | 0.14 ± 0.01 b,c | 0.05 ± 0.001 a | ||
Myco + V | 2.33 ± 0.07 b | 0.32 ± 0.04 b | 0.29 ± 0.02 c | 3.02 ± 0.07 b | 0.16 ± 0.002 b,c | 0.03 ± 0.003 b | ||
Root | Control | 2.29 ± 0.45 b | 0.27 ± 0.09 b | 0.46 ± 0.02 a | 2.90 ± 0.61 b | 0.15 ± 0.03 b,c | 0.02 ± 0.01 a | |
Myco | 4.59 ± 0.29 a | 0.48 ± 0.05 a | 0.57 ± 0.04 a | 5.11 ± 0.32 a | 0.31 ± 0.02 a | 0.03 ± 0.003 a | ||
V | 1.42 ± 0.08 c | 0.17 ± 0.02 c | 0.11 ± 0.04 b | 1.58 ± 0.10 c | 0.13 ± 0.03 c | 0.02 ± 0.005 a | ||
Myco + V | 2.97 ± 0.1 b | 0.37 ± 0.02 a | 0.25 ± 0.03 c | 3.31 ± 0.17 b | 0.21 ± 0.01 b | 0.02 ± 0.001 a | ||
Sorghium | Shoot | Control | 2.28 ± 0.26 b | 0.47 ± 0.05 a | 0.55 ± 0.03 a | 3.38 ± 0.25 b | 0.17 ± 0.01 c | 0.06 ± 0.004 a |
Myco | 4.81 ± 0.31 a | 0.57 ± 0.04 a | 0.54 ± 0.05 a | 6.20 ± 0.41 a | 0.33 ± 0.02 a | 0.07 ± 0.004 a | ||
V | 2.08 ± 0.06 b | 0.36 ± 0.0 b | 0.41 ± 0.01 b | 2.95 ± 0.06 b | 0.14 ± 0.01 c | 0.05 ± 0.003 a | ||
Myco + V | 3.34 ± 0.21 c | 0.53 ± 0.0 a | 0.33 ± 0.01 b | 4.21 ± 0.25 b | 0.23 ± 0.01 b | 0.05 ± 0.002 a | ||
Root | Control | 3.49 ± 0.38 b | 0.38 ± 0.03 a | 0.46 ± 0.01 a,b | 3.89 ± 0.42 b | 0.25 ± 0.03 b | 0.03 ± 0.01 a | |
Myco | 5.51 ± 0.78 a | 0.50 ± 0.07 a | 0.60 ± 0.05 a | 6.12 ± 0.16 a | 0.45 ± 0.02 a | 0.05 ± 0.02 a | ||
V | 2.65 ± 0.08 b | 0.29 ± 0.02 b | 0.11 ± 0.09 c | 2.95 ± 0.09 b | 0.18 ± 0.01 b | 0.02 ± 0.001 a | ||
Myco + V | 3.47 ± 0.46 a,b | 0.34 ± 0.03 a,b | 0.32 ± 0.04 b | 3.85 ± 0.51 b | 0.24 ± 0.03 b | 0.02 ± 0.002 a |
Organ | Treatment | Soluble Sugars | Sucrose | Glucose | Fractose | Insoluble Sugars | Sucrose P Synthase | Invertase | CW Invertase | |
---|---|---|---|---|---|---|---|---|---|---|
Rye | Shoot | Control | 14.8 ± 2.1 c | 5.4 ± 0.7 c | 2.4 ± 0.2 b | 2.4 ± 0.3 d | 213 ± 19 b | 0.6 ± 0.06 d | 12.4 ± 0.1 c | |
Myco | 33.9 ± 1.24 a | 12.3 ± 1.1 a | 3.4 ± 0.8 b | 5.3 ± 0.4 a | 240 ± 17 a | 1.4 ± 0.1 b | 10 ± 0.04 d | |||
V | 20.8 ± 4.22 b | 7.4 ± 1.8 b | 5.2 ± 0.3 a | 3.2 ± 0.03 c | 169 ± 6 c | 0.8 ± 0.07 c | 14.7 ± 0.9 a | |||
Myco + V | 26.3 ± 2.1 b | 13.7 ± 0.5 a | 3.4 ± 0.1 b | 4.2 ± 0.02 b | 215 ± 19 b | 1.6 ± 0.1 a | 11.8 ± 0.1 b | |||
Root | Control | 14.1 ± 1.0 c | 4.1 ± 0.32 b | 1.5 ± 0.12 c | 2.3 ± 0.1 d | 143.3 ± 8 c | 0.6 ± 0.05 c | 1.3 ± 0.08 b | 6.8 ± 0.7 c | |
Myco | 21 ± 1.07 a | 7.7 ± 0.9 a | 2.4 ± 0.15 b | 4.9 ± 0.3 b | 204 ± 12 a | 1.6 ± 0.11 b | 2.3 ± 0.17 a | 14.2 ± 1.05 b | ||
V | 14.5 ± 1.1 c | 5.2 ± 0.4 a,b | 2.2 ± 0.12 b | 3.6 ± 0.3 c | 110.6 ± 9 d | 0.8 ± 0.07 c | 1.1 ± 0.11 b | 11.5 ± 0.8 b | ||
Myco + V | 18.6 ± 1.03 b | 6.8 ± 0.3 a | 3.7 ± 0.1 a | 6.2 ± 0.3 a | 171.8 ± 5 b | 1.9 ± 0.05 a | 2.6 ± 0.08 a | 19.5 ± 1.3 a | ||
Sorghium | Shoot | Control | 22.7 ± 1.4 c | 9.2 ± 1.1 d | 2.3 ± 0.8 c | 4.1 ± 0.4 b | 195.9 ± 2 b | 0.5 ± 0.01 c | 11 ± 0.12 c | |
Myco | 48.8 ± 2.4 a | 14.1 ± 0.9 b | 4.8 ± 0.3 a | 7.7 ± 0.5 a | 226.3 ± 12 a | 1.4 ± 0.01 b | 15.6 ± 0.14 b | |||
V | 29.7 ± 0.9 a,b | 12.6 ± 0.1 c | 2.9 ± 0.1 c | 4.7 ± 0.7 a,b | 157.3 ± 7 c | 0.9 ± 0.4 c | 16.8 ± 0.13 b | |||
Myco + V | 38.3 ± 3.15 b | 18.5 ± 2 a | 4 ± 0.5 b | 6.2 ± 0.1 a | 190 ± 11 b | 1.9 ± 0.1 a | 19.7 ± 0.8 a | |||
Root | Control | 10.9 ± 1 d | 5.2 ± 0.3 c | 1.5 ± 0.1 d | 2.4 ± 0.1 b | 157.7 ± 7 c | 0.8 ± 0.04 b | 1.3 ± 0.09 c | 12.8 ± 0.7 c | |
Myco | 37.2 ± 2 a | 10.5 ± 0.6 a | 3.2 ± 0.2 b | 5.5 ± 0.9 a | 226.9 ± 13 a | 1.6 ± 0.08 a | 2.5 ± 0.1 a | 18.2 ± 0.9 a | ||
V | 14.2 ± 1 c | 7.2 ± 0.4 b | 2 ± 0.14 c | 3.2 ± 0.2 a,b | 115 ± 11 d | 0.7 ± 0.07 b | 1.7 ± 0.13 b | 14.1 ± 1 b,c | ||
Myco + V | 26.7 ± 1 b | 9.7 ± 0.3 a | 4.5 ± 0.1 a | 4.2 ± 0.1 a | 184.2 ± 5 b | 1.4 ± 0.01 a | 2.8 ± 0.0 a | 16.2 ± 0.5 b |
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Selim, S.; Abuelsoud, W.; Alsharari, S.S.; Alowaiesh, B.F.; Al-Sanea, M.M.; Al Jaouni, S.; Madany, M.M.Y.; AbdElgawad, H. Improved Mineral Acquisition, Sugars Metabolism and Redox Status after Mycorrhizal Inoculation Are the Basis for Tolerance to Vanadium Stress in C3 and C4 Grasses. J. Fungi 2021, 7, 915. https://doi.org/10.3390/jof7110915
Selim S, Abuelsoud W, Alsharari SS, Alowaiesh BF, Al-Sanea MM, Al Jaouni S, Madany MMY, AbdElgawad H. Improved Mineral Acquisition, Sugars Metabolism and Redox Status after Mycorrhizal Inoculation Are the Basis for Tolerance to Vanadium Stress in C3 and C4 Grasses. Journal of Fungi. 2021; 7(11):915. https://doi.org/10.3390/jof7110915
Chicago/Turabian StyleSelim, Samy, Walid Abuelsoud, Salam S. Alsharari, Bassam F Alowaiesh, Mohammad M. Al-Sanea, Soad Al Jaouni, Mahmoud M. Y. Madany, and Hamada AbdElgawad. 2021. "Improved Mineral Acquisition, Sugars Metabolism and Redox Status after Mycorrhizal Inoculation Are the Basis for Tolerance to Vanadium Stress in C3 and C4 Grasses" Journal of Fungi 7, no. 11: 915. https://doi.org/10.3390/jof7110915