A tomato MAGIC population reveals candidate genes for leaf dry matter and phenolics, two key traits for stress resilience and climate-smart breeding

Increasing leaf dry matter and phenolic content in tomato has the potential to enhance plant resilience, a key requirement for food security and sustainable agriculture in the context of climate change. However, phenolics accumulation in vegetative tissues remains understudied, as does dry matter accumulation. To address this gap, we leveraged 293 recombinant lines of an eight-way Tomato Multi-Parent Advanced Generation Inter-Cross (ToMAGIC) population to identify candidate genes for leaf dry matter and phenolic content. We found significant variation among lines. Leaf dry matter ranged from 6.90 to 23.20% (CV = 24.84%). Substantial variation was also observed for specialized phenolic metabolites, showing larger differences among lines compared with dry matter. Chlorogenic acid, the most abundant phenolic, ranged from 0.18 to 6.77 g kg^-¹ FW (CV = 76.1%), followed by rutin (0.026-0.352 g kg^-¹ FW, CV = 45.1%), quercetin (0.008-0.141 g kg^-¹ FW, CV = 49.9%), and kaempferol (0.003-0.032 g kg^-¹ FW, CV = 48.8%). Total phenolic content averaged 3.65 g kg^-¹ FW, with nearly a 20-fold range (0.47-8.36 g kg^-¹ FW) (CV = 45.3%). The emergence of highly divergent phenotypes suggests extensive recombination in the population. Traits were highly correlated with each other, with ρ ranging from 0.35 to 0.77, supporting the possibility of indirect selection and suggesting common genetic regulation. Likewise, genomic heritability estimates were moderate to low, where chlorogenic acid presented the highest value (H² = 0.66) and kaempferol the lowest (H² = 0.07). GWAS identified 6 significant associations, explaining 4.50% to 28.24% of the phenotypic variation which, upon further study, enabled the prioritization of candidate genes potentially involved in the control of leaf dry matter and chlorogenic acid content. These findings demonstrate the potential of the ToMAGIC population to facilitate the development of climate-smart tomatoes with improved resilience and reduced input requirements.