Fruit weight regulation by a paralog of Cell Size Regulator (CSR) in tomato and other crops

Fruit weight is a quantitative trait that was under strong selection during the domestication of fruit and vegetable crops such as tomato (Solanum lycopersicum). While numerous fruit weight QTLs have been identified, only three tomato fruit weight genes have been cloned. In this study, we utilized a genetically diverse tomato panel, the Varitome collection, to identify additional genetic loci that control fruit weight. We mapped and fine mapped two fruit weight QTLs on chromosome 6, fw6.1 and fw6.2, by using Genome Wide Association studies (GWAS) and linkage mapping in bi-parental populations. We identified a member of the Cell Size Regulator family, CSR-like1, as the likely candidate underlying fw6.2. The near isogenic lines (NILs) carrying the derived allele of fw6.2 produced heavier fruits with larger fruit pericarp cells than lines with wildtype (WT) allele. Transgenic downregulation of CSR-like1 led to a decrease in fruit weight and pericarp cells, supporting the role of this gene at the fw6.2 locus. The haplotype analysis implied that the CSR-like1-Derived (CSR-like1-D) allele was selected in the transition from the fully wild S. pimpinellifolium to the earliest S. lycopersicum cerasiforme accessions. Four single nucleotide polymorphisms (SNPs) were identified in the regulatory region of CSR-like1 that were conserved in the accessions carrying CSR-like1-WT and were significantly associated with lower fruit weight and pericarp cell size at the locus. Moreover, a pepper GWAS identified a CSR-like1 ortholog that was associated with fruit weight. Together, our findings established CSR-like1 as a novel fruit weight gene likely conserved in other crops in the Solanaceae family.