Physiological and molecular insights into the effect of a seaweed biostimulant on enhancing fruit yield and drought tolerance in tomato

• ANF enhanced plant growth, fruit yield, and drought tolerance in tomatoes. • Transcriptomics reveals ANF activates stress tolerance pathways in tomato leaves. • ANF treatment preserves photosynthesis and delays senescence at molecular level. • Metabolomics shows ANF boosts specific protective metabolites for drought tolerance. • Insights offer a foundation for ANF-based strategies to mitigate climate-related yield loss. Tomato is one of the most widely grown vegetable crops in Europe. This study describes an approach for treating tomato plants with an extract of Ascophyllum nodosum (ANF) prior to a stress event, which prepares the plants at the molecular level to respond more effectively to stress conditions, through a process known as molecular priming. Solanum lycopersicum L. cv. Micro-Tom, a dwarf tomato variety, was pre-treated with ANF via foliar spray during the flowering phase and subsequently subjected to drought conditions. ANF-treated plants exhibited enhanced growth, fruit yield, and stress tolerance under both moderate and severe drought conditions compared to untreated plants. Transcriptomic studies in leaves revealed that the priming treatment preserved the photosynthetic machinery, inducing stress-protective genes involved in ascorbate, peroxidase, GABA, glutathione, and flavanol biosynthesis. Simultaneously, the treatment repressed key senescence-related genes associated with ethylene biosynthesis, as well as several WRKY and NAC transcription factors. Metabolome analysis demonstrated that ANF induces drought tolerance by promoting the accumulation of stress-protective primary and secondary metabolites, such as GABA, proline, maltose, ascorbic acid, quercetin, and biotin, which can act as osmoprotectants and free radical scavengers during drought. Combined transcriptome and metabolome analyses suggest that ANF treatment represses the senescence process, maintains photosynthetic activity, and induces the accumulation of protective metabolites and amino acids, promoting plant survival and growth under drought. Overall, this research provides new insights into the molecular mechanisms underlying biostimulant-based molecular priming and offers a knowledge-based approach for the accurate application of this ANF molecular priming agent to increase crop productivity and mitigate yield loss during drought, contributing to food security in the era of climate change.