Additive multilocus architecture underlies fruit sweetness variation in melon

Abstract Background Fruit sweetness is an important quality trait in melon, but its genetic basis is complex and the mechanisms underlying sweetness variation among elite cultivars remain poorly understood. In particular, the genetic basis of sweetness variation among elite cultivars in the absence of a single major determinant remains unclear. Here, we investigated the genetic architecture of total soluble solids (TSS) by integrating QTL mapping, transcriptomic analysis, and population genomics. Results To investigate the genetic basis of high total soluble solids content, we identified four quantitative trait loci (QTLs) controlling total soluble solids in recombinant inbred populations derived from two Japanese sweet melon cultivars. Each locus exerted modest but reproducible effects, and elevated soluble solids content arose through the cumulative and additive action of multiple alleles rather than through a single major determinant. Although the QTL intervals did not contain known sugar metabolism or transport genes, genes within these intervals were distributed across co-expression modules associated with carbohydrate metabolism. Population genomic analyses revealed only modest and localized genomic signals around these loci and no evidence of strong hard selective sweeps. Conclusions These findings indicate that high sweetness in melon can be established through the accumulation of favorable alleles at multiple loci. Our results explain why variation in fruit sweetness persists even among elite cultivars sharing similar genetic backgrounds and provide a foundation for marker-assisted allele pyramiding to improve fruit sweetness in melon.