Genomic basis of selective breeding from the closest wild relative of large-fruited tomato

The long and intricate domestication history of the tomato (Solanum lycopersicum) includes selection sweeps that have not been fully explored, and these sweeps show significant evolutionary trajectories of domestication traits. Using three distinct selection strategies, we represented comprehensive selected sweeps from 53 Solanum pimpinellifolium (PIM) and 166 S. lycopersicum (BIG) accessions, which are defined as pseudo-domestication in this study. We identified 390 potential selection sweeps, some of which had a significant impact on fruit-related traits and were crucial to the pseudo-domestication process. During tomato pseudo-domestication, we discovered a minor-effect allele of the SlLEA gene related to fruit weight (FW), as well as the major haplotypes of fw2.2/cell number regulator (CNR), fw3.2/SlKLUH, and fw11.3/cell size regulator (CSR) in cultivars. Furthermore, 18 loci were found to be significantly associated with FW and six fruit-related agronomic traits in genome-wide association studies. By examining population differentiation, we identified the causative variation underlying the divergence of fruit flavonoids across the large-fruited tomatoes and validated BRI1-EMS-SUPPRESSOR 1.2 (SlBES1.2), a gene that may affect flavonoid content by modulating the MYB12 expression profile. Our results provide new research routes for the genetic basis of fruit traits and excellent genomic resources for tomato genomics-assisted breeding.

Automated summary

In this study, we conducted comprehensive selection sweeps of 53 tomato varieties and 166 large-fruited tomato germplasm resources using three selection strategies. We identified 390 potential selection sweeps, some of which had significant effects on fruit-related traits and were crucial to the pseudo-domestication process. We also discovered a minor-effect allele of the SlLEA gene related to fruit weight, as well as major haplotypes of fw2.2/CNR, fw3.2/SlKLUH, and fw11.3/CSR in cultivars. Additionally, we found loci significantly associated with fruit weight and six fruit-related agronomic traits through genome-wide association studies. By examining population differentiation, we identified causative variations underlying the divergence of fruit flavonoids and validated the gene SlBES1.2 as a potential regulator of flavonoid content. Our results provide new insights into the genetic basis of fruit traits and valuable genomic resources for tomato genomics-assisted breeding.