Cascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore Manduca sexta L.
Abstract
:1. Introduction
2. Results
2.1. Root Colonization by Rhizophagus irregularis or Trichoderma harzianum Impaired Pupation and Adult Emergence of Manduca sexta Larvae
2.2. Root Colonization by Rhizophagus irregularis or Trichoderma harzianum Altered the Metabolomic Profile of Tomato Leaves
2.3. Root Colonization by Rhizophagus irregularis or Trichoderma harzianum Altered the Metabolic Profile of the Manduca sexta Larval Gut
2.4. Root Colonization by Rhizophagus irregularis or Trichoderma harzianum Altered the Metabolic Profile of the Manduca sexta Larval Fat Body
3. Discussion
4. Materials and Methods
4.1. Plant, Fungal, and Insect Material
4.2. Plant Growth Conditions and Fungal Inoculation
4.3. Rhizophagus irregularis and Trichoderma harzianum Root Colonization
4.4. Bioassay for the Assessment of the Impact of Rhizophagus irregularis and Trichoderma harzianum on Manduca sexta Pupation and Adult Emergence
4.5. Bioassay for the Assessment of the Impact of Rhizophagus irregularis and Trichoderma harzianum on Tomato Leaf Metabolome
4.6. Bioassay to Assess the Impact of Rhizophagus irregularis and Trichoderma harzianum on the Metabolome of Manduca sexta Gut and Fat Body
4.7. Leaf Metabolomics
4.7.1. Extraction of Leaf Metabolites
4.7.2. Liquid Chromatography–Quadrupole Time of Flight–Mass Spectrometry and Data Analysis of the Leaf Extracts
4.8. Dissection of Manduca sexta Larvae and Separation of the Gut and Fat Body Samples
4.9. Insect Metabolomics
4.9.1. Extraction of Metabolites from the Gut and Fat Body of Manduca sexta
4.9.2. Ultra High Performance Liquid Chromatography–Quadrupole Time of Flight–Mass Spectrometry and Data Analysis of the Insect Extracts
4.10. 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 | No Larvae Reaching the Pre-Pupa Stage | Days Until Pre-Pupation (±SD) | Days until Pupation (±SD) | Total No of Pupae | No. of Pupae with Normal Morphology | No. of Pupae with Anomalous Morphology | Weight (g) of Normal Pupae (±SD) | F/M Ratio of the Normal Pupae | Number of Normal Pupae Not Eclosing | No of Moths with Anomalous Morphology | No of Moths with Normal Morphology |
---|---|---|---|---|---|---|---|---|---|---|---|
Non-inoculated | 19 | 23.39 ± 1.47 | 22.06 ± 3.83 | 17 | 13 | 4 | 2.65 ± 0.49 | 9:4 | 2 | 1 | 10 |
R. irregularis | 15 | 20.41 ± 2.54 | 19.94 ± 4.45 | 15 | 11 | 4 | 2.71 ± 0.61 | 3:8 | 3 | 4 | 4 |
T. harzianum | 13 | 22.69 ± 1.9 | 11.61 ± 6.59 | 12 | 5 | 7 | 1.61 ± 0.91 | 2:3 | 1 | 2 | 2 |
One-way ANOVA | - | ns | ns | - | - | - | ns | χ2 = 4.196 | - | - | - |
Feature ID | Annotation | m/z | rt | FC | log2(FC) | Raw p-Value | Level of Confidence |
---|---|---|---|---|---|---|---|
1 | C23H39NO4 | 394.2951 | 12.0 | 5.63 | 2.5 | p < 0.0001 | 3 |
2 | C10H17N3O6S (Glutathione) | 308.0908 | 1.1 | 5.61 | 2.49 | p = 0.0006 | 2 |
3 | C24H41NO3 | 392.3157 | 17.9 | 6.25 | 2.64 | p = 0.002 | 3 |
4 | C23H39NO3 | 378.3012 | 17.4 | 6.56 | 2.71 | p = 0.01 | 3 |
5 | C27H39O3 | 426.3009 | 17.9 | 6.49 | 2.7 | p = 0.04 | 3 |
6 | C5H11N (Piperidine) | 86.0967 | 0.5 | 0.49 | −1.03 | p < 0.0001 | 2 |
7 | C55H94N10O16P2 | 623.3105 | 8.0 | 0.37 | −1.45 | p < 0.0001 | 3 |
8 | C52H97N8O17P3S | 616.3028 | 8.0 | 0.36 | −1.48 | p < 0.0001 | 3 |
9 | No formula | 110.0653 | 1.2 | 0.28 | −1.84 | p < 0.0001 | 4 |
10 | No formula | 132.1018 | 0.4 | 0.49 | −1.03 | p < 0.0001 | 4 |
11 | C12H37N7OS | 328.2841 | 13.1 | 0.02 | −6.05 | p < 0.0001 | 3 |
12 | C23H43N3O6P2 | 520.2708 | 14.9 | 0.02 | −5.76 | p < 0.0001 | 3 |
13 | C14H18N2O5 | 295.1293 | 4.9 | 0.004 | −8.16 | p = 0.002 | 3 |
14 | No formula | 782.0187 | 8.2 | 0.03 | −5.1 | p = 0.001 | 4 |
15 | No formula | 644.2370 | 10.4 | 0.03 | −4.5 | p = 0.003 | 4 |
Feature ID | Annotation | m/z | rt | FC | log2(FC) | Raw p-Value | Level of Confidence |
---|---|---|---|---|---|---|---|
1 | C23H39NO4 | 394.2951 | 12.0 | 378.82 | 8.57 | p < 0.0001 | 3 |
2 | C25H45NO4 (linoleyl-carnitine) | 424.3421 | 13.9 | 597.13 | 9.22 | p < 0.0001 | 2 |
3 | C22H42N2O | 351.3370 | 12.9 | 614.71 | 9.26 | p< 0.0001 | 3 |
4 | No formula | 224.2010 | 9.8 | 388.27 | 8.6 | p < 0.0001 | 4 |
5 | C25H43NO4 (γ-linolenoyl-carnitine) | 422.3274 | 13.2 | 340.61 | 8.41 | p < 0.0001 | 2 |
6 | C23H42NO7P | 476.2772 | 13.0 | 0.19 | −2.4 | p < 0.0001 | 3 |
7 | C13H16N4 | 229.1444 | 7.9 | 0.1 | −3.31 | p < 0.0001 | 3 |
8 | No formula | 110.0653 | 1.2 | 0.2 | −2.34 | p < 0.0001 | 4 |
9 | C8H9NO2 | 152.0709 | 6.7 | 0.05 | −4.34 | p < 0.0001 | 3 |
10 | C10H9NO4 | 225.0872 | 1.3 | 0.16 | −2.67 | p < 0.0001 | 3 |
11 | No formula | 133.0866 | 7.9 | 0.01 | −6.13 | p < 0.0001 | 4 |
12 | No formula | 812.0668 | 8.0 | 0.009 | −6.84 | p < 0.0001 | 4 |
13 | C12H37N7OS | 328.2841 | 13.1 | 0.01 | −6.42 | p < 0.0001 | 3 |
14 | C23H45NO4(O-palmitoyl-carnitine) | 400.3421 | 14.8 | 0.01 | −6.31 | p < 0.0001 | 2 |
15 | C14H18N2O5 | 295.1293 | 4.9 | 0.005 | −7.74 | 0.0001 | 3 |
Feature ID | Annotation | m/z | rt | FC | log2(FC) | p-Value | Level of Confidence |
---|---|---|---|---|---|---|---|
1 | C25H43NO5 | 438.3210 | 11.9 | 3.71 | 1.89 | p < 0.0001 | 3 |
2 | C32H66N4O7P2S | 357.2138 | 6.8 | 3.52 | 1.82 | p < 0.0001 | 3 |
3 | C10H12N2O3 | 209.0909 | 0.9 | 4.73 | 2.24 | p < 0.0001 | 3 |
4 | C37H62N6 | 591.5095 | 15.1 | 3.29 | 1.72 | p < 0.0001 | 3 |
5 | C36H74N2O2 | 567.5823 | 19.9 | 3.64 | 1.87 | p < 0.008 | 3 |
6 | C23H4NO7P | 476.2774 | 11.7 | 0.4 | −1.31 | p < 0.0001 | 3 |
7 | No formula | 175.1163 | 1.1 | 0.37 | −1.42 | p < 0.0001 | 4 |
8 | No formula | 112.0502 | 1.0 | 0.28 | −1.82 | p < 0.0001 | 4 |
9 | No formula | 671.3542 | 5.9 | 0.14 | −2.83 | p < 0.0001 | 4 |
10 | C23H43NO4 (2E)-hexadecenoylcarnitine) | 398.3265 | 13.7 | 0.15 | −2.77 | p < 0.0001 | 2 |
11 | No formula | 224.2010 | 10.0 | 0.05 | −4.42 | p < 0.0001 | 4 |
12 | C37H66N8O10 | 392.2516 | 6.9 | 0.03 | −4.86 | p < 0.0001 | 3 |
13 | C50H94N8O17 | 360.5650 | 6.2 | 0.04 | −4.53 | p < 0.0001 | 3 |
14 | C41H79N14O5PS | 304.5352 | 5.9 | 0.04 | −4.6 | p < 0.0001 | 3 |
15 | C12H37N7OS | 328.2839 | 13.1 | 0.04 | −4.66 | p < 0.0001 | 3 |
Feature ID | Annotation | m/z | rt | FC | log2(FC) | p-Value | Level of Confidence |
---|---|---|---|---|---|---|---|
1 | C9H18O2 | 159.1377 | 12.9 | 6.8 | 2.77 | p < 0.0001 | 3 |
2 | No formula | 320.2558 | 14.5 | 12.36 | 3.63 | p < 0.0001 | 4 |
3 | C17H31NO | 266.2483 | 13.6 | 10.71 | 3.42 | p < 0.0001 | 3 |
4 | C18H37NO (octadecanamide) | 284.295 | 19.6 | 19.24 | 4.27 | p < 0.0001 | 2 |
5 | C36H70N2O4 | 595.5408 | 15.8 | 65.57 | 6.04 | p < 0.0001 | 3 |
6 | C27H50N2O2 | 435.3944 | 17.8 | 105.25 | 6.72 | p < 0.0001 | 3 |
7 | C36H70N2O6 | 627.5310 | 14.9 | 105.4 | 6.72 | p < 0.0001 | 3 |
8 | C28H50N4O8S | 603.3416 | 10.4 | 119.75 | 6.9 | p < 0.0001 | 3 |
9 | C15H41N6O3PS | 417.2771 | 10.6 | 62.57 | 5.97 | p < 0.0001 | 3 |
10 | C23H42NO7P | 476.2774 | 11.7 | 0.21 | −2.24 | p < 0.0001 | 3 |
11 | C44H74N5O10P | 432.7648 | 8.0 | 0.01 | −6.32 | p < 0.0001 | 3 |
12 | C8H16O2 (octanoic acid) | 145.1222 | 8.0 | 0.01 | −6.37 | p < 0.0001 | 2 |
13 | C58H77N31O7 | 660.8389 | 8.0 | 0.008 | −6.93 | p < 0.0001 | 3 |
14 | C35H36N4O7 (benzamide) | 625.2662 | 15.9 | 0.01 | −6.26 | p < 0.0001 | 2 |
15 | No formula | 742.0044 | 7.87 | 0.009 | −6.73 | p < 0.0001 | 4 |
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Papantoniou, D.; Vergara, F.; Weinhold, A.; Quijano, T.; Khakimov, B.; Pattison, D.I.; Bak, S.; van Dam, N.M.; Martínez-Medina, A. Cascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore Manduca sexta L. Metabolites 2021, 11, 731. https://doi.org/10.3390/metabo11110731
Papantoniou D, Vergara F, Weinhold A, Quijano T, Khakimov B, Pattison DI, Bak S, van Dam NM, Martínez-Medina A. Cascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore Manduca sexta L. Metabolites. 2021; 11(11):731. https://doi.org/10.3390/metabo11110731
Chicago/Turabian StylePapantoniou, Dimitra, Fredd Vergara, Alexander Weinhold, Teresa Quijano, Bekzod Khakimov, David I. Pattison, Søren Bak, Nicole M. van Dam, and Ainhoa Martínez-Medina. 2021. "Cascading Effects of Root Microbial Symbiosis on the Development and Metabolome of the Insect Herbivore Manduca sexta L." Metabolites 11, no. 11: 731. https://doi.org/10.3390/metabo11110731