A Citrullus genus super-pangenome reveals extensive variations in wild and cultivated watermelons and sheds light on watermelon evolution and domestication.

Abstract Sweet watermelon ( Citrullus lanatus subsp. vulgaris ) is among the most important vegetable crops in the world. Wild relatives are important resources for watermelon breeding. Here we report high-quality reference genomes of three wild watermelons, C. mucosospermus, C. amarus and C. colocynthis , and the divergence and genome evolution of different Citrullus species. Using genomic data from 547 watermelon accessions spanning four Citrullus species, we construct a super-pangenome to represent the Citrullus gene repertoire and provide a catalogue of orthologous relationships among species. Gene presence/absence variation analysis uncovers many disease resistance genes that are missing in cultivated watermelons, as well as genes with significantly different occurrence frequencies between populations that might underlie watermelon evolution and domestication. We revisit watermelon domestication using the recently identified wild progenitor, Kordofan melon, which provides insights into the domestication of fruit bitterness, sweetness and flesh coloration. The Citrullus super-pangenome provides a valuable resource for breeding and biological discovery, and our comparative genomic analyses shed additional light on watermelon evolution and domestication.