Ecometabolomics for a Better Understanding of Plant Responses and Acclimation to Abiotic Factors Linked to Global Change

Abstract

The number of ecometabolomic studies, which use metabolomic analyses to disentangle organisms' metabolic responses and acclimation to a changing environment, has grown exponentially in recent years. Here, we review the results and conclusions of ecometabolomic studies on the impacts of four main drivers of global change (increasing frequencies of drought episodes, heat stress, increasing atmospheric carbon dioxide (CO₂) concentrations and increasing nitrogen (N) loads) on plant metabolism. Ecometabolomic studies of drought effects confirmed findings of previous target studies, in which most changes in metabolism are characterized by increased concentrations of soluble sugars and carbohydrate derivatives and frequently also by elevated concentrations of free amino acids. Secondary metabolites, especially flavonoids and terpenes, also commonly exhibited increased concentrations when drought intensified. Under heat and increasing N loads, soluble amino acids derived from glutamate and glutamine were the most responsive metabolites. Foliar metabolic responses to elevated atmospheric CO₂ concentrations were dominated by greater production of monosaccharides and associated synthesis of secondary metabolites, such as terpenes, rather than secondary metabolites synthesized along longer sugar pathways involving N-rich precursor molecules, such as those formed from cyclic amino acids and along the shikimate pathway. We suggest that breeding for crop genotypes tolerant to drought and heat stress should be based on their capacity to increase the concentrations of C-rich compounds more than the concentrations of smaller N-rich molecules, such as amino acids. This could facilitate rapid and efficient stress response by reducing protein catabolism without compromising enzymatic capacity or increasing the requirement for re-transcription and de novo biosynthesis of proteins.

Keywords: flavonoids; free amino acids; gas chromatography-mass spectrometry (GC-MS); isoflavonoids; liquid chromatography-mass spectrometry (LC-MS); phenolics; proton nuclear magnetic resonance spectrometry (1H-NMR); shikimate acid; soluble sugars; terpenes.

Figure 1

Shifts in principal plant metabolites and metabolic pathways in response to drought conditions reported in 81 ecometabolomic studies. The numbers within the squares are the numbers of reports describing changes in photosynthetic tissue metabolite concentration and/or pathway activity under drought stress. Red numbers within red squares indicate significant increases; black numbers within black squares indicate significant decreases. Red arrows indicate upregulation of the metabolic pathway; bold black arrows indicate no changes.

Figure 2

Shifts in principal plant metabolites and metabolic pathways in response to heat stress reported in 22 ecometabolomic studies. The numbers within the squares are the numbers of reports describing changes in photosynthetic tissue metabolite concentration and/or pathway activity under heat stress. Red numbers within red squares indicate significant increases; black numbers within black squares indicate significant decreases. Red arrows indicate upregulation of the metabolic pathway.

Figure 3

Shifts in principal plant metabolites and metabolic pathways in response to increased atmospheric CO₂ concentrations reported in 17 ecometabolomic studies. The numbers within the squares are the numbers of reports describing changes in photosynthetic tissue metabolite concentration and/or pathway activity under elevated atmospheric CO₂ concentrations. Red numbers within red squares indicate significant increases; black numbers within black squares indicate significant decreases. Red arrows indicate upregulation of the metabolic pathway.

Figure 4

Shifts in principal plant metabolites and metabolic pathways in response to increased N loads reported in eight ecometabolomic studies. The numbers within the squares are the numbers of reports describing changes in photosynthetic tissue metabolite concentration and/or pathway activity under higher N loads. Red numbers within red squares indicate significant increases; black numbers within black squares indicate significant decreases. Red arrows indicate upregulation of the metabolic pathway. Blue arrows indicate downregulation of the metabolic pathway.