Metabolic network divergence: polyamine and ethylene dynamics in Arabidopsis thaliana and Solanum lycopersicum

Abstract

Polyamines are ubiquitously present in all living organisms. In plants, together with phytohormone ethylene, their metabolism plays a crucial role in plant stress and ontogenesis. We have evaluated differences in the responses of model plants Arabidopsis thaliana and Solanum lycopersicum to abiotic stresses and metabolic modulators based on key metabolite levels. Previous approaches have often focused separately on either polyamines, amino acids, or ethylene precursors. As these pathways are directly interconnected, their simultaneous evaluation can significantly impact our understanding of their core mechanisms. We have therefore developed a novel and validated liquid chromatography - tandem mass spectrometry based method, enabling quantification of fourteen compounds: the amino acids L-arginine, L-citrulline, L-ornithine; biogenic amines N-acetyl-L-ornithine and agmatine; the polyamines putrescine, spermidine, spermine, thermospermine, N-acetylputrescine, cadaverine, homospermidine; together with methionine and 1-aminocyclopropane-1-carboxylic acid, serving as key non-volatile precursors of ethylene. Our analysis revealed distinct metabolic responses between Arabidopsis and tomato, highlighted by species-specific differences in polyamine metabolism and ethylene precursors dynamics. Drought and salinity stresses triggered fundamentally different metabolic adjustments, with drought consistently inducing higher metabolite levels and spermine showing stress-specific responses. Metabolic inhibitor treatments with aminoguanidine and L-norvaline revealed further divergencies, mainly demonstrated as significant variations in ethylene precursor levels. For all approaches, Arabidopsis displayed more pronounced metabolic fluctuations compared to tomato. These results provide direct insights into contrasting metabolic plasticity and the interconnected roles of polyamines, amino acids, and ethylene precursors in plant responses and adaptations.