Novel loci fsd6.1 and Csgl3 regulate ultra-high fruit spine density in cucumber.

KEY MESSAGE: Quantitative Trait Loci (QTL) analysis of multiple populations in multiple environments revealed that the fsd6.2 locus, which includes the candidate gene Csgl3, controls high fruit spine density in natural cucumbers. GWAS identified a novel locus fsd6.1, which regulates ultra-high fruit spine density in combination with Csgl3, and evolved during cucumber domestication. Fruit spine density, a domestication trait, largely influences the commercial value of cucumbers. However, the molecular basis of fruit spine density in cucumber remains unclear. In this study, four populations were derived from five materials, which included three with low fruit spine density, one with high fruit spine density, and one with ultra-high fruit spine density. Fruit spine densities were measured in 15 environments over a span of 6 years. The distributions were bimodal suggesting that fruit spine density is controlled by a major-effect QTL. QTL analysis determined that the same major-effect QTL, fsd6.2, is present in four populations. Fine mapping indicated that Csgl3 is the candidate gene at the fsd6.2 locus. Phylogenetic and geographical distribution analyses revealed that Csgl3 originated from China, which has the highest genetic diversity for fruit spine density. One novel minor-effect QTL, fsd6.1, was detected in the HR and HP populations derived from the cross between 65G and 02245. In addition, GWAS identified a novel locus that colocates with fsd6.1. Inspection of a candidate region of about 18 kb in size using pairwise LD correlations, combined with genetic diversity and phylogenetic analysis of fsd6.1 in natural populations, indicated that Csa6G421750 is the candidate gene responsible for ultra-high fruit spine density in cucumber. This study provides new insights into the origin of fruit spine density and the evolution of high/ultra-high fruit spine density during cucumber domestication.