Interspecific tomato MAGIC rootstocks confer drought tolerance through distinct biochemical and transcriptomic modulation.

Abstract

Drought stress is a major constraint for tomato production, affecting plant water status, growth, and physiological performance. Grafting onto genetically diverse rootstocks offers a promising strategy to improve drought adaptation. Based on previous evaluations, interspecific tomato MAGIC-derived lines (ToMAGIC) showing contrasting drought responses were selected as candidate tolerant and susceptible genotypes. We hypothesized that these contrasting genotypes would differentially modulate the drought response of a grafted Moneymaker scion when used as rootstock, and that the selected tolerant lines would confer improved performance through distinct physiological and biochemical responses associated with rootstock-specific transcriptional regulation. To test this hypothesis, Moneymaker scions were grafted onto six rootstocks, including three selected lines from the interspecific ToMAGIC population, and evaluated using six biological replicates per treatment under control conditions or after 10 days water withholding treatment. Phenotypic and biochemical traits were assessed, and RNA sequencing was performed on scion leaf tissue. Rootstock genotype strongly influenced the drought response of the scion. Under the 10-day water-withholding treatment, S5_T_583 and S5_T_724 showed more favorable performance, while self-grafted Moneymaker and S5_T_865 exhibited more pronounced stress symptoms. S5_T_583 maintained 14% higher leaf water content and 11% higher root water content than the commercial rootstock Emperador under water stress, while reducing the mean wilting score from 3.0 to 0.5. It also accumulated approximately threefold more total flavonoids and two fold more total phenolic compounds than Emperador. S5_T_724 also maintained approximately 9% higher leaf and root water content than Emperador and showed a lower wilting score. RNA-seq and WGCNA revealed rootstock-specific gene-expression patterns and co-expression modules associated with photosynthesis, protein processing in the endoplasmic reticulum, carotenoid biosynthesis, phenylalanine metabolism, amino acid metabolism, nitrogen metabolism, and lipid metabolism. These findings indicate that selected ToMAGIC-derived rootstocks improve drought response in grafted tomato through distinct physiological and biochemical responses associated with rootstock-specific transcriptional patterns.