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

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 Nα-acetyl-l-ornithine and agmatine; the polyamines putrescine, spermidine, spermine, thermospermine, N-acetylputrescine, cadaverine, homospermidine; together with l-methionine and 1-aminocyclopropane-1-carboxylic acid, serving as 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 modulator treatments with aminoguanidine and l-norvaline, targeting polyamine catabolism and biosynthesis, respectively, revealed further divergencies, mainly demonstrated as significant variations in ethylene precursor levels. Additional experiments with Arabidopsis mutants affected in ethylene synthesis and arginine metabolism pathways, as well as methionine treatment, further confirmed the interconnected nature of these metabolic networks and their responses to pathway perturbations. 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.