Abstract
The cyst nematodes Heterodera schachtii and Heterodera trifolii, whose major hosts are sugar beet and clover, respectively, damage a broad range of plants, resulting in significant economic losses. Nematodes synthesize metabolites for organismal development and social communication. We performed metabolic profiling of H. schachtii and H. trifolii in the egg, juvenile 2 (J2), and female stages. In all, 392 peaks were analyzed by capillary electrophoresis time-of-flight mass spectrometry, which revealed a lot of similarities among metabolomes. Aromatic amino acid metabolism, carbohydrate metabolism, choline metabolism, methionine salvage pathway, glutamate metabolism, urea cycle, glycolysis, gluconeogenesis, coenzyme metabolism, purine metabolism, pyrimidine metabolism, and tricarboxylic acid (TCA) cycle for energy conversion (β-oxidation and branched-chain amino acid metabolism) energy storage were involved in all stages studied. The egg and female stages synthesized higher levels of metabolites compared to the J2 stage. The key metabolites detected were glycerol, guanosine, hydroxyproline, citric acid, phosphorylcholine, and the essential amino acids Phe, Leu, Ser, and Val. Metabolites, such as hydroxyproline, acetylcholine, serotonin, glutathione, and glutathione disulfide, which are associated with growth and reproduction, mobility, and neurotransmission, predominated in the J2 stage. Other metabolites, such as SAM, 3PSer, 3-ureidopropionic acid, CTP, UDP, UTP, 3-hydroxy-3-methylglutaric acid, 2-amino-2-(hydroxymethyl-1,3-propanediol, 2-hydroxy-4-methylvaleric acid, Gly Asp, glucuronic acid-3 + galacturonic acid-3 Ser-Glu, citrulline, and γ-Glu-Asn, were highly detected in the egg stage. Meanwhile, nicotinamide, 3-PG, F6P, Cys, ADP-Ribose, Ru5P, S7P, IMP, DAP, diethanolamine, p-Hydroxybenzoic acid, and γ-Glu-Arg_divalent were unique to the J2 stage. Formiminoglutamic acid, nicotinaminde riboside + XC0089, putrescine, thiamine 2,3-dihydroxybenzoic acid, 3-methyladenine, caffeic acid, ferulic acid, m-hydrobenzoic acid, o- and p-coumaric acid, and shikimic acid were specific to the female stage. Overall, highly similar identities and quantities of metabolites between the corresponding stages of the two species of nematode were observed. Our results will be a valuable resource for further studies of physiological changes related to the development of nematodes and nematode–plant interactions.
Highlights
Nematodes, arguably one of the largest groups of animals, cause significant agricultural losses and human diseases [1,2]
The peaks were annotated based on the Human Metabolome Technology (HMT) (Yamagata, Japan) standard library and KnownUnknown peak library based on m/z values and migration time (MT)
The bioanalytical techniques used for metabolomics studies include, but are not limited to, LC-MS, GC-MS and NMR spectroscopy
Summary
Arguably one of the largest groups of animals, cause significant agricultural losses and human diseases [1,2]. Heterodera schachtii is considered a major pest in sugar beet production. It parasitizes more than 200 plant species, most notably the Chenopodiaceae and Cruciferae families [3]. Heterodera trifolii is a dark brown, large-cyst nematode with a cone top structure and a strong under-bridge with a sheaf-like organ in the center and heavily furcated ends within the fenestral area. It has a wide host range, including Trifolium, Medicago, Lespedeza, Glycine, Dianthus, Lotus, Vinca, Melilotus, Spinacea, Polygonum, Rumex, Chenopodium, Agrostis pai, Curcuma larga, Solanum, Pisum, and Phaseolus [6]. H. schachtii and H. trifolii have morphological resemblances, host range similarityies and exhibit similar symptoms of damage; this makes it difficult to distinguish between these species in the field [7,8]
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