Dissecting the genetic architecture and plasticity of the fruit primary metabolome in a Solanum habrochaites introgression library under contrasting nutrient regimes

This is the authors' abstract. We don't add key points for this paper.

Optimizing nutrient use efficiency while maintaining fruit quality is a central challenge for sustainable tomato breeding. This study leverages 53 chromosome segment substitution lines (CSSLs) derived from a cross between cultivated tomato and the wild relative Solanum habrochaites (LA1777) to explore the genetic and metabolic basis of adaptation to varying nutrient availability. The CSSLs were evaluated under high-input (HI) and low-input (LI) regimes and characterized for their agro-qualitative performances and primary metabolome profiles. Gas chromatography-mass spectrometry identified 63 compounds revealing a significant metabolic variability driven by input conditions. The plastic response of metabolites highlighted a shift in the accumulation of fruit's carbon- and nitrogen-related compounds: HI conditions enhanced amino acids levels, whereas the LI regime prioritized carbon-rich compounds, resulting in increased sugar content. Using a 51K SNP array, the population was mapped at high resolution across 2614 BINs covering 68% of the genome. Metabolic QTL (mQTL) analysis using stepwise regression and 1000 permutations identified 81 high-confidence loci, including pleiotropic regions on chromosomes 1, 3, and 4 that were associated with amino and organic acid metabolism, corresponding to conserved regions across wild tomato species. Analysis of candidate genes revealed that specific genomic regions responsive to LI govern abiotic stress resistance, while stable hotspots across nutrient regimes highlight the presence of highly canalized genetic hubs. The integration of mapping data with previously identified mQTL and transcriptomic studies validates the biological relevance of these identified loci in coordinating nutrient stress responses and fruit metabolic adaptation. Several lines demonstrated superior metabolite accumulation under stress and varying degrees of plasticity, making them ideal candidates for breeding. These findings provide a high-resolution framework for marker-assisted selection to develop climate-resilient, high-quality tomato cultivars optimized for sustainable agriculture.