Phylogenomic and super-pangenome analyses unveil the genetic landscape of tomato evolution and domestication

The tomato (Solanum lycopersicum L.), a principal fruit crop, exhibits significant genetic diversity shaped by domestication and breeding. Analysis of the gene-based super-pangenome, a catalogue of all genes across diverse genome-sequenced tomatoes, has not yet been fully explored. Here, we present a comprehensive analysis of the gene-based super-pangenome across 61 genetically diverse tomato varieties, revealing 59 066 orthologous groups, thereby providing a detailed genetic framework for understanding the evolution of tomatoes. Our phylogenetic analysis recalibrates the position of S. galapagense, challenging existing paradigms of tomato evolution. Identification of genes linked to key agronomic traits such as fruit size, ripening and stress tolerance, along with their presence/absence variation among accessions, offers a rich source of genetic markers for breeding programs. The study also highlights the impact of whole-genome triplication (WGT) and tandem gene duplication (TD) events on gene family expansion, particularly in distant wild relatives. The analysis of the LRR-RLK gene family, important for plant development and defence, reveals substantial sequence diversity and conservation. Rapidly evolving genes and those under positive selection, such as HAI3, CYP711A1/MAX1, WRKY9 and CNGC15, are implicated in stress tolerance and defence mechanisms. The identification of these genes, along with specific pathogenesis-related genes in distant wild relatives, suggests potential strategies to improve fruit shelf life, fruit set and stress tolerance in elite tomato cultivar breeding. Additionally, we have developed the tomatoPangenome platform, integrating genomic and pangenomic data, gene families and tools, to support sustainable production of high-quality, climate-resilient tomatoes and advance selective breeding for future food security.