Metabolic Analysis of the Development of the Plant-Parasitic Cyst Nematodes Heterodera schachtii and Heterodera trifolii by Capillary Electrophoresis Time-of-Flight Mass Spectrometry
Abstract
:1. Introduction
2. Results
2.1. Data Collection
2.2. Major Metabolic Biosynthetic Pathways in Nematode Species
2.3. Relative Peak Areas of Metabolites and Patterns of Variation across the Stages
2.4. Highly Detected Metabolites in Nematode Species
2.5. Pearson’s Correlation and Multivariate Analysis of Metabolic Profiles
2.6. Heat Map and Biological Properties of Stage-Specific Metabolites
3. Discussion
4. Materials and Methods
4.1. Sample Preparation
4.2. CE-TOF/MS Analysis of Metabolites
4.3. Data Processing and Analysis
4.4. Statistical Analysis
4.5. Plotting on the Pathway Map
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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HS-E | HS-J2 | HS-F | HT-E | HT-J2 | HT-F | |
---|---|---|---|---|---|---|
HS-E | 1 | |||||
HS-J2 | 0.8203 * | 1 | ||||
HS-F | 0.9417 * | 0.8450 * | 1 | |||
HT-E | 0.9545 * | 0.8594 * | 0.9357 * | 1 | ||
HT-J2 | 0.7975 * | 0.9651 * | 0.8103 * | 0.8394 * | 1 | |
HT-F | 0.8008 * | 0.7545 * | 0.8814 * | 0.8509 * | 0.7481 * | 1 |
Stage | Metabolites with No Significant Difference between HS and HT | Metabolites Significantly Higher in HS than HT | Metabolites Significantly Higher in HT than HS |
---|---|---|---|
Egg | XC0120, Leu-Leu-Tyr, Lauric acid, Spermine, dCMP, Val-Pro-Pro, Gly-Asp, N-Methylproline, γ-Glu-Ile + γ-Glu-Leu, Glycerol 2-phosphate, Dimethylaminoethanol, dATP, Decanoic acid, N-Acetylhistidine, N-Acetylalanine, Pyridoxamine-P, 2-Methylserine, dADP, ATP, Dyphylline, Octanoic acid, dTMP, XC0071, Hexanoic acid, Pantothenic acid, N-Acetylaspartic acid, N-Acetylmethionine, Citric acid, XC0126, γ-Glu-Ornitine, cis-Hydroxyproline, 2-Aminoisobutyric acid + 2-Aminobutyric acid, Thymidine, Asn, Pelargonic acid, S7P, XA0065, Lys, γ-Glu-Gln, Leu, XA0017, γ-Glu-Ala, Ile, Isocitric acid, γ-Glu, Asn, Val, Gly-Gly, 8-Hydroxyoctanoic acid + 2-Hydroxyoctanoic acid, Tyr, Aminoacetone, 1-Methylhistidine + 3-Methylhistidine, dAMP, γ-Glu-Lys, β-Hydroxyisovaleric acid, NADP+, γ-Glu-Asp, ADP, Carnitine, Triethanolamine, Terephthalic acid, p-Toluic acid + m-Toluic acid+ o-Toluic acid, 4-Oxopyrrolidine-2-carboxylic acid, Ser, dGuanosine, NAD+, Glu, γ-Glu-Ser, CDP-choline, γ-Glu-Val, AMP, MTA, Tetrahydrouridine, N-Acetyllysine, N-Acetylserine, ADMA, ADP-Glc + GDP-fucose, Isobutylamine, Glycerol, Heptanoic acid, O-Succinylhomoserine, cAMP, Theobromine, 11-Aminoundecanoic acid, N-Acetylglucosylamine, 7-Methylguanine, FAD, Xanthosine, Azelaic acid, Diethanolamine, UTP, Glucaric acid, and 5-MTHF | Citrulline, Methionine sulfoxide, Urocanic acid, XC0132, Penicillamine, XC0065, MIA, Choline, 3-PG, Thiamine, Myoinositol 1-phosphate + Myoinositol 3-phosphate, Imidazole-4-acetic acid, CTP, PEP, Ethanolamine, Ophthalmic acid, CDP, GlcNAc-P, Myoinositol 2-phosphate, G1P, Ser-Glu, Acetylcholine, 5-Hydroxylysine, TMP, Putrescine, XC0016, Arg-Glu, Octanoylcarnitine, 3-Methyladenine, CMP, NAcGlcNP, 3-Hydroxy-3-methylglutaric acid, 3′,5′-ADP, 2-Deoxyglucose 6-phosphate, XA0033, Phosphorylcholine, 6-PG, Arg, 6-Hydroxyhexanoic acid, 2-Hydroxy-4-methylvaleric acid, Riboflavin, Ru5P, γ-Glu-Arg, XA0019, GSSG, Cysteine glutathione disulfide, 4-GBA, Ornithine, Inosine, EAP, Gln, Threonic acid, Cystathionine, Betaine, Cystine, 7-Methylxanthine, ThPP, His-Glu, γ-Glu-Thr, N-Acetylgalactosamine + ManNA + GlcNAc, IMP, XC0089 + Nicotinamide riboside, GABA, 3-Hydroxy-2-methyl-4-pyrone, Thr, GMP, Hydroxyproline, and FMN | Adenine, S-Methylmethionine, Cys, Hypotaurine, Uracil, 2-Hydroxyglutaric acid, trans-Glutaconic acid, b β-Cyanoalanine, Thiaproline, Quinic acid, Actinine, 1-Methyladenosine, Pipecolic acid, Glucuronic acid-1 + Galacturonic acid-1, Dihydrouracil, S-Methylcysteine, UDP-GlcA, N1-Methylguanosine, Glucuronic acid-2 + Galacturonic acid-2, 3-Aminoisobutyric acid, Isovalerylcarnitine, γ-Glu-Cys, GSH, 3-HBA, Oxoproline, β-Ala, Lactic acid, Succinic acid, Mevalonic acid, Adenosine, S-Methylglutathione, Malic acid, dcSAM, Mucic acid, O-Acetylhomoserine + 2-Aminoadipic acid, Fumaric acid, 3-Ureidopropionic acid, SDMA, Daminozide + Ala-Ala, 1,5-Gluconolactone, Succinyl AMP, γ-Glu-Citrulline, Glucuronic acid-3 + Galacturonic acid-3, Guanine, CoA, γ-Glu-His, 1-Aminocyclopropane-1-carboxylic acid +, Homoserinelactone, UDP, SAHC, Saccharopine, N6-Acetyllysine, Mevalolactone, 2-OG, DOPA, NicRN, F6P, GDP, N8-Acetylspermidine, O-Acetylserine, Gluconic acid, N1-Acetylspermidine, Gly, Homogentisic acid + p-Hydroxymandelic acid, F1,6P, ALCAR, p-Hydroxybenzoic acid, G6P, SAM, 3PSer, N6, Methyllysine, Ala, Nω-Methylarginine, Met, Trp, G3P, GPCho, Pro, γ-Glu-Phe, Asp, γ-Glu-Gly, Spermidine, Phe, 3′-AMP, GTP, dGTP, UMP, cis-Aconitic acid, Uridine, Nicotinic acid, Homoserine, Trimethyllysine, His, Guanosine, and γ-Glu-Met |
J2 | p-Toluic acid + m-Toluic acid + o-Toluic acid, Myoinositol 2-phosphate, XA0017, XC0071, Dihydrouracil, XC0065, ThPP, Xanthine, TMP, dTMP, GPCho, Gluconic acid, 3-PG, γ-Glu-Asn, Penciclovir, Spermidine, Formiminoglutamic acid, XA0004, Pantothenic acid, CMP, γ-Glu-Asp, Asn, Lactic acid, Uridine, Betaine, Tyr-Glu, Kynurenic acid, 2-Deoxyglucose 6-phosphate, Terephthalic acid, Cystine, 3′-CMP + 2′-CMP, Nω-Methylarginine, Guanine, Heptanoic acid, Isobutylamine, o-Coumaric acid + p-Coumaric acid, G3P, Kynurenine, UMP, 1,5-Gluconolactone, GMP, SAHC, 5-Hydroxylysine, Serotonin, 3′,5′-ADP, 2-PG, Spermine, Cysteine glutathione disulfide, GSSG, His-Glu, Aminoacetone, Octanoic acid, γ-Glu-Met, Oxoproline, ATP, SAM, γ-Glu-Gly, GTP, Fumaric acid, Guanosine, Inosine, Quinic acid, 3PSer, Isethionic acid, Adenosine, Hexanoic acid, Lys, 3-Hydroxy-2-methyl-4-pyrone, Ophthalmic acid, Glycerol, ADMA, S7P, AMP, UDP, Ser, dcSAM, N-Acetylgalactosamine + ManNAc + GlcNAc, 3-Mercaptolactic acid, 2-Hydroxyglutaric acid, 1-Methylhistidine + 3-Methylhistidine, XA0019, 11-Aminoundecanoic acid, trans-Glutaconic acid, Citraconic acid, p-Hydroxybenzoic acid, Acetylcholine, N-Acetylmethionine, Pelargonic acid, ADP, Theobromine, XC0089 + Nicotinamide riboside, Leu, 3-Hydroxy-3-methylglutaric acid, N-Acetylglucosylamine, Tyr, γ-Glu-His, Lauric acid, N6-Methyllysine, NAcGlcNP, Lauroylcarnitine, Malic acid, Arg, Decanoic acid, γ-Glu-Ile + γ-Glu-Leu, Glu, ADP-Glc + GDP-fucose, BTL, FAD, γ-Glu-Lys, CoA, PEP, γ-Glu-Gln, Glucuronic acid-3 + Galacturonic acid-3, GABA, 1H-Imidazole-4-propionic acid, His, Orotidine, γ-Glu, Phe, 3′-AMP, Uric acid, 3-Aminoisobutyric acid, DHAP, Pretonine, γ-Glu-Ser, N-Acetylalanine, XC0126, Succinyl AMP, Ascorbate 2-glucoside, Mucic acid, Thiaproline, Diethanolamine, and Agmatine | O-Acetylhomoserine + 2-Aminoadipic acid, ADP-Rib, Nicotinamide, Myoinositol 1-phosphate + Myoinositol 3-phosphate, Asp, Butyrylcarnitine, Putrescine, Thiamine, Hypoxanthine, Tyr-Arg_divalent, Acetylserine, Allantoic acid, Homoserine, IMP, UDP-GlcA, 4-GBA, Pipecolic acid, XC0040, Cadaverine, Methionine sulfoxide, Arg-Glu, F1,6P, MTA, Riboflavin, N-Acetylhistidine, Gly-Asp, 2-Methylserine, Nicotinic acid, 2,3-Diaminopropionic acid, cGMP, Ethanolamine, GDP, Octanoylcarnitine, XA0065, 2-Hydroxy-4-methylvaleric acid, G6P, F6P, 3-HBA, γ-Glu-Thr, Propionylcarnitine + XC0061, Trimethyllysine, dGuanosine, N-Acetylserine, Thr, Urocanic acid, XA0033, Ser-Glu, G1P, Sucrose 6′-phosphate, MIA, XC0016, Actinine, Pyridoxamine-P, β-Cyanoalanine, Phosphorylcholine, FMN, Citrulline, Cystathionine, Met, CDP-choline, Phe, Thymidine, 7-Methylxanthine, EAP, Saccharopine, Gln, and Adenine | 1-Methyladenosine, N6-Acetyllysine, N-Methylproline, Octopamine + Dopamine, N1-Methylguanosine, S-Methylcysteine, S-Methylglutathione, Pterin, XC0132, DOPA, Xanthosine, Sebacic acid, Pro, 3-Methyladenine, γ-Glu-Cys, γ-Glu-Ala, N1-Acetylspermidine, Glucuronic acid-2 + Galacturonic acid-2, γ-Glu-Arg, Suberic acid, 2-OG, NAD+, 6-PG, SDMA, Cys, Homogentisic acid + p-Hydroxymandelic acid, Isovalerylcarnitine, Threonic acid, Succinic acid, Ru5P, N8-Acetylspermidine, 7-Methylguanine, PRPP, GSH, Hydroxyproline, Trp, cis-Hydroxyproline, Ile, Leu-Leu-Tyr, N-Formylkynurenine, GlcNAc-P, Biopterin, NicRN, Ala, Citric acid, Val, R5P, NADP+, γ-Glu-Val, ALCAR, Ornithine, 2-Aminoisobutyric acid + 2-Aminobutyric acid, Dyphylline, β-Ala, Choline, Gly, 4-Oxopyrrolidine-2-carboxylic acid, Azelaic acid, and Carnitine |
Female | GDP, 6-PG, Stachydrine, BTL, XC0017, Sebacic acid, Isobutyric acid + Butyric acid, Glycerol, Azetidine 2-carboxylic acid, Ectoine, Myoinositol 2-phosphate, G1P, 11-Aminoundecanoic acid, β-Hydroxyisovaleric acid, Putrescine, FAD, Agmatine, Azelaic acid, Cystine, Deamido-NAD, Asp, γ-Glu-Citrulline, Dyphylline, R5P, UMP, MTA, 2-Hydroxyvaleric acid, dAdenosine + 5′-Deoxyadenosine, Hexanoic acid, CDP-choline, 4-GBA, Val, Pro-Pro, Cysteic acid, Biopterin, Isovaleric acid + DL-2-Methylbutyric acid + Valeric acid, GTP, Hypoxanthine, NADP+, XC0120, N-Acetylalanine, dcSAM, Tetrahydrouridine, Betaine, Diethanolamine, 3′,5′-ADP, 3-Methyladenine, Ru5P, Threonic acid, γ-Glu-Arg, NAD+, cGMP, UTP, NicRN, Xanthosine, Pimelic acid, ArgSuccinate, AMP, N6-Acetyllysine, Glycerol 2-phosphate, Pyruvic acid, Leu, Ophthalmic acid, N-Acetylserine, Galactosamine + Glucosamine, 3-Methoxytyrosine, Theobromine, Pyridoxal, Isobutylamine, Arg, 1-Aminocyclopropane-1-carboxylic acid + Homoserinelactone, ADP, SAHC, 7,8-Dihydrobiopterin, Ile, Asn, dTMP, Decanoic acid, 3-Ureidopropionic acid, Octanoylcarnitine, Choline, Gln, S-Methylmethionine, 3PSer, N-Acetyllysine, S7P, G3P, γ-Glu-Met, cis-Hydroxyproline, F1,6P, Leu-Leu-Tyr, cAMP, N-Acetylglucosylamine, 2-Methylserine, N-AcGlu, γ-Glu-Ornitine, Lauric acid, F6P, 3-Mercaptolactic acid, Terephthalic acid, Hexylamine, XA0017, Pterin, Glutaric acid + Methylsuccinic acid, p-Hydroxybenzoic acid, GPCho, 7-Methylguanine, Octanoic acid, XA0019, UDP, m-Hydroxybenzoic acid, Propionylcarnitine + XC0061, 5-Oxohexanoic acid, Pyridoxamine, 3′-CMP + 2′-CMP, N-Acetylaspartic acid, Pelargonic acid, Glucaric acid, p-Toluic acid + m-Toluic acid + o-Toluic acid, His-Glu, 3-Guanidinopropionic acid, Mevalolactone, and γ-Glu-Asp | Thiamine, MIA, Dimethylaminoethanol, Urocanic acid, N-Methylputrescine, Citrulline, 2-Deoxyglucose 6-phosphate, 5-Hydroxypentanoic acid, XC0065, Nicotinamide, Cadaverine, Myoinositol 1-phosphate + Myoinositol 3-phosphate, XA0033, 2-Hydroxy-4-methylvaleric acid, GSSG, Ethanolamine, TMP, Glyceric acid, Phosphorylcholine, Ornithine, GlcNAc-P, CTP, Penicillamine, CDP, 3-Methylguanine, 8-Hydroxyoctanoic acid, o-Hydroxybenzoic acid, 3-Hydroxy-3-methylglutaric acid, 3-PG, XC0132, CMP, NAcGlcNP, EAP, Inosine, ThPP, Riboflavin, Methionine sulfoxide, dCMP, XA0065, Nicotinic acid, Guanosine, ADP-Glc + GDP-fucose, PEP, Trehalose 6-phosphate, Met, GMP, Pyridoxamine-P, Gly-Asp, XC0040, FMN, IMP, 5-Hydroxylysine, Cysteine glutathione disulfide, Cystathionine, ATP, dGuanosine, Actinine, Uric acid, and Uridine | Ferulic acid, o-Coumaric acid + p-Coumaric acid, GSH, Allantoic acid, Adenine, 1-Methyladenosine, 2,3-Diaminopropionic acid, Shikimic acid, DOPA, Guanine, Homogentisic acid + p-Hydroxymandelic acid, Pipecolic acid, Mucic acid, Tyr, 2-Hydroxyglutaric acid, γ-Glu-Gly, SDMA, Indole-3-carboxylic acid, S-Methylcysteine, O-Acetylhomoserine + 2-Aminoadipic acid, Saccharopine, Succinyl AMP, γ-Glu-His, ADMA, Sulfotyrosine, Formiminoglutamic acid, γ-Glu-Asn, Isovalerylcarnitine, Citraconic acid, Trp, Glucuronic acid-1 + Galacturonic acid-1, N1-Methylguanosine, Ser-Glu, γ-Glu-Ser, XC0089 + Nicotinamide riboside, 3-Aminoisobutyric acid, Succinic acid, Adenosine, trans-Glutaconic acid, γ-Glu-Thr, trans-Cinnamic acid, Quinic acid, Isethionic acid, DHMA, γ-Glu-Phe, N-Formylkynurenine, O-Acetylserine, Phe, Lys, XC0126, Gly-Gly, S-Methylglutathione, Ascorbate 2-glucoside, Malic acid, S-Carboxymethylcysteine, Fumaric acid, XC0016, Carnitine, XC0071, ALCAR, Pyridoxine, Nω-Methylarginine, N1-Acetylspermidine, γ-Glu-Val, Pro, Aminoacetone, N6-Methyllysine, N5-Ethylglutamine, N8-Acetylspermidine, Oxoproline, Thiaproline, γ-Glu-Gln, Triethanolamine, γ-Glu-Ile + γ-Glu-Leu, Arg-Glu, γ-Glu-Lys, Carboxymethyllysine, γ-Glu-Ala, N-Methylproline, Mevalonic acid, 3′-AMP, Kynurenine, 3-HBA, UDP-GlcA, Homoserine, Imidazole-4-acetic acid, His, Spermidine, Hydroxyproline, β-Ala, Isocitric acid, β-Cyanoalanine, Heptanoic acid, GABA, 2-OG, Metronidazole Glucuronic acid-3 + Galacturonic acid-3, G6P, Trimethyllysine, Citric acid, cis-Aconitic acid, Glucuronic acid-2 + Galacturonic acid-2, BAPN, N-Acetylgalactosamine + ManNAc + GlcNAc, 7-Methylxanthine, Lactic acid, 2-Aminoisobutyric acid + 2-Aminobutyric acid, Spermine, 2,3-Dihydroxybenzoic acid, Ala, Dihydrouracil, Homocitrulline, Phosphoramidon, 1-Methylhistidine + 3-Methylhistidine, Val, Gly, Gluconic acid, Thr, XA0004, 1,5-Gluconolactone, Thymidine, SAM, Uracil, Pantothenic acid, Ser, 4-Oxopyrrolidine-2-carboxylic acid, Glu, and 3-Hydroxy-2-methyl-4-pyrone |
Sample Name | Replicates | Dried Extract (mg) | Solvent (ACN:H2O;1:1) (µL) |
---|---|---|---|
H. schachtii Egg | HS-egg-1 | 24.6 | 1200 |
HS-egg-2 | 27.9 | 1200 | |
HS-egg-3 | 27.4 | 1200 | |
H. schachtii Juvenile-2 | HS-J2-1 | 20.8 | 900 |
HS-J2-2 | 28.3 | 1200 | |
HS-J2-3 | 24.9 | 1200 | |
H. schachtii Female | HS-F-1 | 25.1 | 1200 |
HS-F-2 | 19.1 | 900 | |
HS-F-3 | 27.5 | 1200 | |
H. trifolii Egg | HT-egg-1 | 20.7 | 900 |
HT-egg-2 | 26.1 | 1200 | |
HT-egg-3 | 25.3 | 1200 | |
H. trifolii Juvenile-2 | HT-J2-1 | 22.5 | 900 |
HT-J2-2 | 29.7 | 1200 | |
HT-J2-3 | 30.1 | 1500 | |
H. trifolii Female | HT-F-1 | 24.7 | 1200 |
HT-F-2 | 14.4 | 600 | |
HT-F-3 | 12.3 | 600 |
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Assefa, A.D.; Kim, S.-H.; Mani, V.; Ko, H.-R.; Hahn, B.-S. Metabolic Analysis of the Development of the Plant-Parasitic Cyst Nematodes Heterodera schachtii and Heterodera trifolii by Capillary Electrophoresis Time-of-Flight Mass Spectrometry. Int. J. Mol. Sci. 2021, 22, 10488. https://doi.org/10.3390/ijms221910488
Assefa AD, Kim S-H, Mani V, Ko H-R, Hahn B-S. Metabolic Analysis of the Development of the Plant-Parasitic Cyst Nematodes Heterodera schachtii and Heterodera trifolii by Capillary Electrophoresis Time-of-Flight Mass Spectrometry. International Journal of Molecular Sciences. 2021; 22(19):10488. https://doi.org/10.3390/ijms221910488
Chicago/Turabian StyleAssefa, Awraris Derbie, Seong-Hoon Kim, Vimalraj Mani, Hyoung-Rai Ko, and Bum-Soo Hahn. 2021. "Metabolic Analysis of the Development of the Plant-Parasitic Cyst Nematodes Heterodera schachtii and Heterodera trifolii by Capillary Electrophoresis Time-of-Flight Mass Spectrometry" International Journal of Molecular Sciences 22, no. 19: 10488. https://doi.org/10.3390/ijms221910488