Pangenome-resolved structural variation drives adaptation and trait evolution in cucumber

Abstract

Cucumber (Cucumis sativus L.) is a global vegetable crop and powerful model for sex determination, fruit development and vascular biology. We present high-quality genome assemblies for 125 cultivated and wild accessions, capturing worldwide genetic diversity. Syntenic gene family analysis characterized 37,897 gene families and revealed haplotype diversity shaped by geographic expansion. Comparative analyses uncovered copy-number variations linked to local adaptation, including a CsFT tandem duplication promoting early flowering at higher latitudes. This resource reduces reference bias, enabling the annotation of resistance loci and the discovery of CsCcu, a nucleotide-binding leucine-rich repeat-type R gene conferring scab resistance. We cataloged 135,597 structural variations and quantified their regulatory effects, with ~30% driving trait diversification among geographic groups. Integrating structural variations into genome-wide association studies identified 172 quantitative trait loci for 38 agronomic traits, including a rare long terminal repeat insertion regulating fruit length via CsSPL1. Our findings provide a genomic toolkit for cucumber evolution research and precision breeding. Pangenome analyses of chromosome-scale genome assemblies for 125 diverse cucumber accessions highlight structural variation shaped by selection for geographical adaptation, fruit-length diversification and disease resistance.