A wild Cucurbita genome reveals the role of structural variants and introgression in domestication

Abstract

Despite their economic importance and well-characterized domestication syndrome, the genomic impact of domestication and the identification of variants underlying the domestication traits in Cucurbita species (pumpkins and squashes) is currently lacking. Cucurbita argyrosperma, also known as cushaw pumpkin or silver-seed gourd, is a Mexican crop consumed primarily for its seeds rather than fruit flesh. This makes it a good model to study Cucurbita domestication, as seeds were an essential component of early Mesoamerican diet and likely the first targets of human-guided selection in pumpkins and squashes. We obtained population-level data using tunable Genotype by Sequencing libraries for 192 individuals of the wild and domesticated subspecies of C. argyrosperma across Mexico. We also assembled the first wild Cucurbita genome at a chromosome level. Comparative genomic analyses revealed several structural variants and presence/absence of genes related to domestication. Our results indicate a monophyletic origin of this domesticated crop in the lowlands of Jalisco. We uncovered candidate domestication genes that are involved in the synthesis and regulation of growth hormones, plant defense mechanisms, flowering time and seed development. The presence of shared selected alleles with the closely related species Cucurbita moschata suggests domestication-related introgression between both taxa.