Methionine Triggers Metabolic, Transcriptional, and Epigenetic Reprogramming in Arabidopsis Leaves

Abstract

Methionine (Met) is a central metabolite in plants, as it serves as a precursor for S-adenosylmethionine (SAM), a key methyl donor for epigenetic and metabolic processes. Met is also an essential amino acid that limits the nutritional value of plant-based diets. Understanding how altered Met levels affect the metabolome, transcriptome, and epigenetic regulation of plant leaves remains an open challenge. This study investigates the impact of ectopic Met accumulation in SSE Arabidopsis leaves of transgenic lines expressing a deregulated form of AtCGS (AtD-CGS) under the seed-specific phaseolin promoter. Unexpected activation of the phaseolin promoter in leaves led to AtD-CGS expression and variable Met accumulation among progeny, despite genetic homozygosity. High-Met (HM) plants showed elevated amino acid and sugar levels, enrichment of stress-related transcripts, and suppression of Met biosynthetic genes, while Low-Met (LM) plants showed reduced Met levels and increased non-CG DNA methylation, especially in centromeric and promoter regions. Integrated transcriptome and methylome analyses revealed that high Met levels were associated with the upregulation of stress hormone pathways (abscisic acid, jasmonate, salicylic acid, and ethylene), downregulation of key epigenetic regulators (e.g., MET1, CMTs), and broader transcriptional reprogramming. By contrast, low Met (LM) lines displayed similar expression levels of genes as control plants. Our findings reveal a complex regulatory network whereby Met accumulation reprograms metabolism, gene expression, and DNA methylation patterns. These results suggest feedback between sulfur-carbon metabolism, stress adaptation, and epigenetic control, positioning Met as both a nutrient and a signaling hub in plant physiology.