Foliar Application of Bio-Stimulants Enhancing the Production and the Toxicity of Origanum majorana Essential Oils Against Four Rice Seed-Borne Fungi
Abstract
:1. Introduction
2. Results and Discussion
2.1. Field Study
2.1.1. Effects of Ascorbic Acid, Tryptophan and Moringa Leaf Extract on Vegetative Growth
2.1.2. Effects of Ascorbic Acid, Tryptophan and Moringa Extract on the Chemical Parameters of O. majorana
Oil Percentage (%)
Total Chlorophyll and Carbohydrate Content
Chemical Composition of the Essential Oils
2.2. In Vitro Study
2.2.1. Isolation and Identification of the Fungal Isolates
2.2.2. Molecular Identification through the Internal Transcribed Spacer (ITS) Region
2.3. Antifungal Activity of Essential Oils
2.4. Efficacy of Seed Treatment with Essential Oils Against Seed-Borne Fungi
3. Materials and Methods
3.1. Preparation of Aqueous Extracts of Moringa Oleifera, Ascorbic Acid and Tryptophan
3.2. Field Study
3.3. Vegetative Growth and Chemical Parameters
3.4. Extraction of the Essential Oils
3.5. GC/MS Analysis of the Essential Oils
3.6. In Vitro Study for Fungal Isolation
3.7. In Vitro Study for Fungal Identification
3.7.1. Culture Characteristics and Microscopic Examination
3.7.2. Molecular Identification through the Internal Transcribed Spacer (ITS) Region
3.7.3. Sequencing of the Amplified ITS Region
3.8. Antifungal Activity and Minimum Inhibitory Concentration (MIC) Assays of Essential Oils (First Investigation)
3.9. Efficacy of Seed Treatment with Selected Essential Oils Against Seed-Borne Fungi (Second Investigation)
3.10. Statistical Analysis
4. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Sample Availability: Samples of the compounds are not available from the authors. |
Treatments | Plant Height (cm) | Plant Diameter (cm) | Branch Number | Leaf Fresh Weight (g) | Leaf Dry Weight (g) | Leaf Area | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
2018 | 2019 | 2018 | 2019 | 2018 | 2019 | 2018 | 2019 | 2018 | 2019 | 2018 | 2019 | |
Control | 17.16 d* ± 1.87 | 23.16 b ± 3.95 | 21.33 b ± 0.76 | 26.00 e ± 1.39 | 95.16 b ± 8.54 | 143.50 c ± 14.23 | 29.62 e ± 1.92 | 51.86 c ± 0.23 | 11.55 b ± 4.29 | 12.42 d ± 1.01 | 0.323 f ± 0.030 | 0.453 d ± 0.063 |
AA 100 mg/L | 20.00 ab ± 1.39 | 25.66 ab ± 2.46 | 23.58 ab ± 0.76 | 29.50 ab ± 0.25 | 150.00 a ± 15.78 | 223.00 a ± 13.61 | 35.77 abc ± 1.45 | 60.68 ab ± 6.73 | 19.11 ab ± 1.82 | 21.20 abc ± 4.83 | 0.431 becd ± 0.114 | 0.713 ab ± 0.135 |
AA 200 mg/L | 20.66 ab ± 3.12 | 27.08 a ± 3.95 | 23.66 ab ± 2.75 | 30.41 ab ± 0.52 | 150.33 a ± 8.69 | 230.16 a ± 59.25 | 37.56 ab ± 6.29 | 64.12 a ± 2.02 | 19.41 ab ± 6.74 | 21.57 ab ± 7.14 | 0.365 ef ± 0.012 | 0.412 d ± 0.034 |
AA 300 mg/L | 21.33 a ± 2.24 | 27.08 a ± 3.16 | 24.75 a ± 0.66 | 31.08 a ± 0.62 | 152.33 a ± 9.50 | 232.16 a ± 10.39 | 39.08 a ± 6.29 | 64.37 a ± 2.68 | 20.72 a ± 5.62 | 25.03 a ± 4.79 | 0.733 a ± 0.053 | 0.852 a ± 0.07 |
Trp 100 mg/L | 19.58 abc ± 4.15 | 25.33 ab ± 2.50 | 22.50 ab ± 1.56 | 27.33 cde ± 0.38 | 139.83 a ± 6.00 | 214.50 ab ± 36.87 | 30.24 de ± 1.34 | 54.20 bc ± 3.25 | 11.97 b ± 4.88 | 13.42 cd ± 1.31 | 0.392 cedf ± 0.025 | 0.458 cd ± 0.051 |
Trp 200 mg/L | 19.75 abc ± 0.66 | 25.50 ab ± 3.27 | 22.58 ab ± 0.52 | 28.66bcd ± 0.2 | 143.00 a ± 7.54 | 219.00 a ± 38.50 | 30.61 cde ± 1.88 | 54.96 bc ± 8.56 | 12.48 b ± 0.86 | 14.90 bcd ± 5.47 | 0.517 b ± 0.120 | 0.611 bc ± 0.084 |
Trp 300 mg/L | 19.75 abc ± 2.17 | 25.50 ab ± 1.80 | 23.25 ab ± 4.02 | 28.83 bc ± 1.84 | 145.16 a ± 4.53 | 221.50 a ± 21.21 | 31.12 cde ± 3.00 | 57.09 abc ± 3.18 | 13.41 ab ± 2.55 | 15.56 bcd ± 1.06 | 0.474 cbd ± 0.036 | 0.61 bc ± 0.045 |
MLE 2.5% | 17.91 cd ± 1.75 | 24.33 b ± 2.02 | 21.91 b ± 1.28 | 26.66 de ± 3.35 | 107.16 b ± 26.27 | 168.16 bc ± 13.32 | 32.54 bcde ± 0.85 | 58.08 abc ± 2.26 | 13.47 ab ± 7.26 | 16.93 bcd ± 5.50 | 0.385 def ± 0.006 | 0.477 cd ± 0.077 |
MLE 5% | 18.75 bcd ± 2.61 | 24.50 ab ± 2.00 | 22.41 ab ± 1.18 | 26.75 de ± 1.14 | 136.83 a ± 17.32 | 209.16 ab ± 20.93 | 33.77 abcde ± 1.98 | 58.66 abc ± 5.03 | 15.46 ab ± 1.28 | 17.22 abcd ± 7.69 | 0.5 bc ± 0.080 | 0.741 ab ± 0.035 |
MLE 10% | 19.66 abc ± 1.25 | 24.91 ab ± 3.18 | 22.41 ab ± 0.80 | 27.08 cde ± 0.52 | 138.16 a ± 31.60 | 213.66 ab ± 14.15 | 35.37 abcd ± 0.27 | 59.06 abc ± 3.37 | 16.39 ab ± 5.97 | 20.09 abcd ± 4.27 | 0.497 bc ± 0.0155 | 0.669 b ± 0.190 |
Treatment | Total Chlorophyll Content (SPAD) | Total Carbohydrate Content (%) | Oil Percentage (%) | |||
---|---|---|---|---|---|---|
2018 | 2019 | 2018 | 2019 | 2018 | 2019 | |
Control | 44.68 c* ± 10.10 | 47.66 c ± 10.80 | 7.50 f ± 0.45 | 7.66 g ± 0.47 | 0.664 b ± 0.050 | 0.658 abc ± 0.219 |
AA 100 mg/L | 53.13 abc ± 3.07 | 54.05 bc ± 4.29 | 8.71 c ± 0.46 | 8.86 d ± 0.47 | 0.892 ab ± 0.168 | 0.535 c ± 0.128 |
AA 200 mg/L | 57.01 abc ± 11.93 | 58.10 abc ± 5.96 | 8.81 c ± 0.45 | 9.04 c ± 0.44 | 0.864 ab ± 0.094 | 0.546 bc ± 0.178 |
AA 300 mg/L | 57.71 ab ± 2.86 | 58.08 abc ± 3.28 | 8.86 c ± 0.47 | 9.08 c ± 0.45 | 0.982 a ± 0.462 | 0.737 abc ± 0.240 |
Trp 100 mg/L | 45.33 c ± 14.07 | 51.31 bc ± 8.58 | 8.01 e ± 0.45 | 8.42 e ± 0.45 | 0.726 ab ± 0.199 | 0.683 abc ± 0.148 |
Trp 200 mg/L | 47.06 bc ± 3.79 | 53.53 bc ± 2.91 | 8.06 e ± 0.45 | 7.98 f ± 0.45 | 0.8 ab ± 0.156 | 0.826 a ± 0.245 |
Trp 300 mg/L | 52.55 abc ± 1.16 | 53.90 bc ± 3.51 | 8.37 d ± 0.44 | 8.44 e ± 0.40 | 0.748 ab ± 0.054 | 0.822 ab ± 0.148 |
MLE 2.5% | 56.03 abc ± 5.04 | 60.11 ab ± 4.23 | 9.10 b ± 0.45 | 9.10 c ± 0.45 | 0.977 ab ± 0.218 | 0.799 abc ± 0.017 |
MLE 5% | 56.28 abc ± 8.14 | 60.68 ab ± 11.48 | 9.73 a ± 0.15 | 9.29 b ± 0.45 | 0.917 ab ± 0.127 | 0.81 abc ± 0.146 |
MLE 10% | 59.90 a ± 7.20 | 66.36 a ± 8.31 | 9.62 a ± 0.30 | 9.79 a ± 0.15 | 1.065 a ± 0.313 | 0.867 a ± 0.058 |
Percentage in the Oil (%) | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|
Compound Name | Control (Untreated Plants) | AA (mg/L) | MLE (%) | Trp (mg/L) | ||||||
100 | 200 | 300 | 2.5 | 5 | 10 | 100 | 200 | 300 | ||
α-Pinene | 0.53 (913,910) * | 0.41 (937,921) | 0.61 (916,910) | ND | 0.68 (914,911) | ND | ND | ND | ND | 0.45 (920,914) |
Sabinene | 6.83 (863,861) | 8.66 (878,876) | 7.82 (877,876) | 5.49 (918,909) | 6.89 (917,911) | 2.76 (937,930) | 3.13 (932,924) | 5.79 (918,917) | 3.53 (929,928) | 6.67 (935,929) |
α-Terpinene | 0.42 (927,923) | ND | 0.84 (908,907) | 0.33 (923,919) | 3.55 (909,907) | ND | 0.8 (923,919) | 0.7 (921,905) | ND | ND |
2-Carene | ND | 2.9 (881,881) | 1.42 (886,885) | 0.73 (869,864) | ND | ND | 0.61 (868,867) | ND | ND | ND |
Cymene | 4.5 (865,850) | 3.83 (846,809) | 4.55 (864,846) | 3.29 (829,813) | 3.9 (906,888) | 3.53 (914,903) | 3.04 (929,909) | 4.41 (824,815) | 7.2 (893,875) | 17.75 (896,884) |
γ-Terpinene | 1.56 (930,925) | 4.88 (898,869) | 3.17 (901,875) | 2.53 (934,928) | 7.65 (887,885) | 0.96 (938,930) | 2.84 (931,926) | 2.53 (931,926) | 0.67 (938,930) | 0.32 (881,877) |
4-Thujanol (Sabinene hydrate) | 10.51 (885,884) | 11.3 (865,865) | 10.38 (875,874) | 12.18 (866,862) | 24.47 (867,865) | 46.47 (847,845) | 33.28 (873,871) | 37.17 (911,908) | 39.88 (865,862) | 9.13 (925,915) |
Terpineol (cis-β-(1-Terpinenol)) | 33.17 (814,812) | 26.76 (856,839) | 28.44 (803,787) | 38.06 (820,806) | ND | ND | ND | ND | ND | ND |
cis-p-2-Menthen-1-ol | 1.29 (874,871) | 1.2 (874,870) | 1.4 (877,873) | 1.09 (876,875) | 1.29 (892,887) | 1.39 (887,835) | 2 (902,896) | 1.68 (882,878) | 1.68 (878,872) | ND |
Terpinen-4-ol | 22.25 (813,813) | 21.58 (815,815) | 21.73 (824,824) | 17.42 (837,837) | 33.34 (815,815) | 27.65 (870,864) | 32.04 (829,829) | 26.09 (822,822) | 25.9 (819,818) | 38.35 (902,896) |
cis-Piperitol | 0.23 (847,800) | 0.19 (845,806) | 0.22 (856,814) | 0.12 (839,790) | 0.18 (884,841) | 0.18 (920,893) | 0.27 (897,877) | 0.21 (870,829) | 0.27 (871,811) | 1.82 (858,831) |
α-Terpineol | 7.78 (824,765) | 6.24 (861,827) | 7.37 (860,814) | 7.18 (847,815) | 8.88 (857,857) | 9.48 (884,883) | 12.58 (842,832) | 10.67 (821,772) | 9.22 (873,873) | 7.91 (933,921) |
Linalyl acetate | 2.33 (846,845) | ND | 2.41 (819,817) | 2.45 (822,821) | 0.76 (907,903) | 1.86 (933,930) | 1.01 (926,923) | 0.92 (897,895) | 3.72 (862,858) | ND |
cis-Sabinene hydrate acetate | 2.24 (852,811) | 5.06 (867,780) | 2.09 (870,825) | 1.91 (885,786) | 3.64 (888,789) | 0.33 (925,818) | 1.7 (913,811) | 2.88 (922,877) | 2.03 (888,790) | 0.86 (922,859) |
1-Terpinen-4-yl acetate | 0.35 (838,830) | 0.48 (846,838) | 0.54 (822,814) | 0.32 (906,862) | 0.34 (842,833) | 0.27 (867,855) | 0.67 (836,828) | 0.41 (850,841) | 0.55 (838,829) | ND |
2,5-Dimethyl-3-hexyne-2,5-diol | 0.62 (796,757) | 0.32 (810,766) | 0.53 (794,758) | 0.19 (807,757) | 0.21 (822,780) | 0.36 (823,786) | 0.15 (819,771) | 0.53 (822,782) | 0.36 (817,779) | ND |
Caryophyllene | 2.26 (894,850) | 2.71 (812,810) | 3.19 (865,806) | 2.71 (812,809) | 2.1 (899,870) | 1.84 (918,918) | 2.02 (913,903) | 2.01 (891,862) | 1.96 (890,866) | 1.46 (915,913) |
γ-Elemene | 0.61 (863,860) | 1.16 (840,839) | 0.96 (837,835) | 1.36 (840,839) | 0.82 (857,855) | 0.53 (869,865) | 0.91 (846,844) | 0.83 (860,858) | 0.42 (878,874) | ND |
(-)-Spathulenol | 0.72 (863,862) | 0.7 (888,873) | 0.75 (859,859) | 0.67 (900,882) | 0.23 (885,883) | 0.75 (921,906) | 0.61 (915,902) | 0.88 (865,864) | 0.84 (906,889) | 4.52 (901,900) |
Caryophyllene oxide | 0.22 (886,884) | 0.19 (884,882) | 0.21 (904,903) | 0.29 (884,881) | 0.09 (916,912) | 0.43 (935,933) | 0.33 (922,921) | 0.16 (926,924) | 0.41 (916,915) | 0.29 (776,762) |
Monoterpenes (%) | 94.61 | 93.81 | 93.52 | 93.29 | 95.78 | 95.24 | 94.12 | 93.99 | 95.01 | 83.26 |
Sesquiterpenes (%) | 3.81 | 4.76 | 5.11 | 5.03 | 3.24 | 3.55 | 3.87 | 3.88 | 3.63 | 6.27 |
Non- oxygenated constituents (%) | 16.71 | 24.55 | 22.56 | 16.44 | 25.59 | 9.62 | 13.35 | 16.27 | 13.78 | 26.65 |
Oxygenated constituents (%) | 81.71 | 74.02 | 76.07 | 81.88 | 73.43 | 89.17 | 84.64 | 81.60 | 84.86 | 62.88 |
Control | AA 100 mg/L | AA 200 mg/L | AA 300 mg/L | MLE 2.5% | MLE 5% | MLE 10% | Trp 100 mg/L | Trp 200 mg/L | Trp 300 mg/L | |
---|---|---|---|---|---|---|---|---|---|---|
Control | 1 | |||||||||
AA 100 mg/L | 0.99 | 1 | ||||||||
AA 200 mg/L | 0.997 | 0.999 | 1 | |||||||
AA 300 mg/L | 1.000 | 0.991 | 0.995 | 1 | ||||||
MLE 2.5% | 0.989 | 0.999 | 0.997 | 0.985 | 1 | |||||
MLE 5% | 0.996 | 0.980 | 0.987 | 0.998 | 0.972 | 1 | ||||
MLE 10% | 0.999 | 0.987 | 0.993 | 1.000 | 0.980 | 0.999 | 1 | |||
Trp 100 mg/L | 1.000 | 0.993 | 0.997 | 1.000 | 0.988 | 0.997 | 0.999 | 1 | ||
Trp 200 mg/L | 0.999 | 0.989 | 0.994 | 1.000 | 0.983 | 0.999 | 1.000 | 1.000 | 1 | |
Trp 300 mg/L | 0.963 | 0.985 | 0.977 | 0.955 | 0.990 | 0.937 | 0.949 | 0.962 | 0.954 | 1 |
Isolate Code | Cultivar | Isolated Fungi | Accession Number | Reference |
---|---|---|---|---|
F.g.101 | Sakha 101 | Fusarium graminearum | MK450469 | [58] |
F.v.101 | Fusarium verticilliodies | MK450470 | [58] | |
B.o.177 | Giza 177 | Bipolaris oryzae | MK450473 | [58] |
C.l.177 | Curvularia lunata | MK450466 | (This study) |
Oil from Plant Treated with | Inhibition Percentage % | |||
---|---|---|---|---|
F. verticilliodies | F. graminearum | B. oryzae | C. lunata | |
Control (without oil) | 0.00 f ± 0.00 * | 0.00 e ± 0.00 | 0.00 f ± 0.00 | 0.00 e ± 0.00 |
Control (oil from untreated plants) | 63.56 e ± 0.77 | 62.87 d ± 0.37 | 45.83 e ± 1.65 | 50.74 d ± 0.74 |
AA (100 mg/L) | 70.93 cd ± 0.67 | 70.07 b ± 1.00 | 77.65 bcd ± 1.65 | 74.07 b ± 0.97 |
AA (200 mg/L) | 69.76 b ± 0.67 | 70.07 b ± 1.00 | 80.68 abc ± 1.73 | 81.85 a ± 0.97 |
AA (300 mg/L) | 69.76 bc ± 0.67 | 68.18 bc ± 0.65 | 82.19 ab ± 3.23 | 81.11 a ± 0.64 |
Trp (100 mg/L) | 65.50 de ± 1.39 | 67.80 cd ± 4.60 | 75.37 d ± 1.00 | 70.74 c ± 0.97 |
Trp (200 mg/L) | 67.82 cd ± 1.02 | 82.19 a ± 2.10 | 77.65 bcd ± 1.36 | 72.59 bc ± 1.33 |
Trp (300 mg/L) | 71.31 b ± 0.38 | 85.60 a ± 0.75 | 79.54 abcd ± 0.65 | 74.81 b ± 1.95 |
MLE (2.5%) | 65.11 de ± 1.34 | 63.25 cd ± 2.00 | 76.13 cd ± 0.65 | 73.70 bc ± 0.74 |
MLE (5%) | 94.57 a ± 1.39 | 70.07 b ± 0.37 | 79.54 abcd ± 0.65 | 73.70 bc ± 0.97 |
MLE (10%) | 92.63 a ± 0.38 | 71.96 b ± 0.37 | 84.46 a ± 3.10 | 75.18 b ± 1.33 |
Mancozeb (200 mg/L) ** | 53.5 ± 2.45 | 65.15 ± 2.62 | 77.35 ± 2.54 | 63.33 ± 3.33 |
Oil from Plant Treated with | Minimum Inhibitory Concentration (MIC mg/L) | |||
---|---|---|---|---|
F. verticilliodies | F. graminearum | B. oryzae | C. lunata | |
Control (Oil from untreated plants) | 300 | 300 | 400 | 400 |
AA (100 mg/L) | 350 | 350 | 250 | 350 |
AA (200 mg/L) | 350 | 350 | 250 | 250 |
AA (300 mg/L) | 350 | 350 | 250 | 250 |
Trp (100 mg/L) | 300 | 350 | 350 | 350 |
Trp (200 mg/L) | 350 | 250 | 250 | 350 |
Trp (300 mg/L) | 350 | 250 | 250 | 350 |
MLE (2.5%) | 300 | 300 | 250 | 350 |
MLE (5%) | 200 | 350 | 250 | 350 |
MLE (10%) | 200 | 350 | 250 | 350 |
Mancozeb(reference fungicide) | 40 | 30 | 20 | 25 |
Fungi | Seeds without Oil | Oils from Plants Treated with | |||
---|---|---|---|---|---|
Untreated Plants | Ascorbic Acid (300 mg/L) | Moringa Extract (10%) | Tryptophan (300 mg/L) | ||
F. verticilliodies | 28 | 24 | 0.0 | 0.0 | 0.0 |
F. graminearum | 21 | 18 | 42 | 0.0 | 0.0 |
B. oryzae | 232 | 32 | 0.0 | 70 | 7.0 |
C. lunata | 49 | 0.0 | 0.0 | 0.0 | 0.0 |
Total grains | |||||
Healthy grains | 70 | 326 | 358 | 330 | 393 |
Infected grains | 330 | 74 | 42 | 70 | 7 |
Rice grain infection (%) | 82.5 | 18.5 | 10.5 | 17.5 | 1.75 |
Season | pH | EC (dSm−1) | Soluble Cations (meq/L) | Soluble Anions (meq/L) | |||||
---|---|---|---|---|---|---|---|---|---|
Ca++ | Mg++ | Na+ | K+ | HCO3− | Cl− | SO2−− | |||
2018 | 8.08 | 2.53 | 18.20 | 14.20 | 23.91 | 4.49 | 7.20 | 21.00 | 27.10 |
2019 | 8.13 | 2.03 | 13.22 | 3.0 | 16.21 | 3.79 | 6.52 | 16.93 | 25.21 |
Treatment | Concentration | Treatment | Concentration |
---|---|---|---|
Control plants | Tap water | Trp | 200 mg/L |
AA (ascorbic acid) | 100 mg/L | Trp | 300 mg/L |
AA | 200 mg/L | (moringa leaf extract) MLE | 2.5% |
AA | 300 mg/L | MLE | 5% |
Trp (tryptophan) | 100 mg/L | MLE | 10% |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
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Mohamed, A.A.; El-Hefny, M.; El-Shanhorey, N.A.; Ali, H.M. Foliar Application of Bio-Stimulants Enhancing the Production and the Toxicity of Origanum majorana Essential Oils Against Four Rice Seed-Borne Fungi. Molecules 2020, 25, 2363. https://doi.org/10.3390/molecules25102363
Mohamed AA, El-Hefny M, El-Shanhorey NA, Ali HM. Foliar Application of Bio-Stimulants Enhancing the Production and the Toxicity of Origanum majorana Essential Oils Against Four Rice Seed-Borne Fungi. Molecules. 2020; 25(10):2363. https://doi.org/10.3390/molecules25102363
Chicago/Turabian StyleMohamed, Abeer A., Mervat El-Hefny, Nader A. El-Shanhorey, and Hayssam M. Ali. 2020. "Foliar Application of Bio-Stimulants Enhancing the Production and the Toxicity of Origanum majorana Essential Oils Against Four Rice Seed-Borne Fungi" Molecules 25, no. 10: 2363. https://doi.org/10.3390/molecules25102363