Ecometabolomics of plant-herbivore and plant-fungi interactions: a synthesis study

The functional adaptive responses of higher plants to biotic interactions with herbivores and fungi have long been topics of research. One constraint to obtaining a comprehensive understanding of the most general plant responses, however, has been the difficulty of studying all plant functional shifts simultaneously due to analytical limitations. Now this is possible with the advent of metabolomics. Using 151 records from the WEB of SCIENCE database, we have analyzed the development and application of metabolomic profiles to ecological studies in the last two decades. We have used meta-analysis and pathway enrichment analyses to assess the whole set of constitutive and inducible defenses. Constitutive defenses against herbivores were mainly based on a significant high level of the metabolism of several amino acids with parallel increases in the concentrations of flavones (phenolics) and saponins (glycosides). Inducible defenses, though, were mainly based on the increases in concentration of methyl-ketone, pantothenate, and Coenzyme A. Butyrate metabolism and the mitochondrial electron-transport chain were upregulated, in agreement with previous reports that herbivory-activated plant chemical defenses were mainly based on jasmonic acid, salicylic acid, and ethylene-associated pathways. The metabolic responses/acclimations to pathogenic fungi were mainly linked with increases in aspartate and pyruvate metabolism, the transfer of acetyl groups within mitochondria, and the upregulation of branched-chain amino acids degradation pathways. These responses/acclimations were accompanied by higher concentrations of the most important groups of secondary metabolites such as phenolics (anthocyanins, flavonoids), quinones, alkaloids, terpenoids, and polyamines and other compounds related to antistress mechanisms such as proline. The leaves of mycorrhized plants accumulated nucleotide sugars, sphingolipids, and methylhistidine. These responses were associated with maintaining the integrity of plant cell membranes under fungal hypha penetration. The responses were accompanied by increases in the concentrations of phenolics, blumenols, and alkaloids and decreases in the concentrations of polyamines, consistent with the mycorrhizal inhibition of polyamines. This summary provides a clear synthesis of the most successful plant strategies selected after millions of years of evolution and will be a very promising tool for the management of crops and ecosystems and for selecting the main lines in breeding studies for future research.

Automated summary

Research on plant responses to biotic interactions with herbivores and fungi using metabolomics reveals that constitutive defenses are related to amino acid metabolism and the concentrations of flavones and saponins, while inducible defenses are mainly linked to increases in methyl-ketone, pantothenate, and Coenzyme A concentrations. Metabolic responses to pathogenic fungi are associated with aspartate and pyruvate metabolism, acetyl group transfer within mitochondria, and branched-chain amino acids degradation pathways, accompanied by increases in concentrations of secondary metabolites such as phenolics and decreases in polyamines.