A chromosome-level genome of a Kordofan melon illuminates the origin of domesticated watermelons

Wild relatives or progenitors of crops are important resources for breeding and for understanding domestication. Identifying them, however, is difficult because of extinction, hybridization, and the challenge of distinguishing them from feral forms. Here, we use collection-based systematics, iconography, and resequenced accessions of Citrullus lanatus and other species of Citrullus to search for the potential progenitor of the domesticated watermelon. A Sudanese form with nonbitter whitish pulp, known as the Kordofan melon (C. lanatus subsp. cordophanus), appears to be the closest relative of domesticated watermelons and a possible progenitor, consistent with newly interpreted Egyptian tomb paintings that suggest that the watermelon may have been consumed in the Nile Valley as a dessert by 4360 BP. To gain insights into the genetic changes that occurred from the progenitor to the domesticated watermelon, we assembled and annotated the genome of a Kordofan melon at the chromosome level, using a combination of Pacific Biosciences and Illumina sequencing as well as Hi-C mapping technologies. The genetic signature of bitterness loss is present in the Kordofan melon genome, but the red fruit flesh color only became fixed in the domesticated watermelon. We detected 15,824 genome structural variants (SVs) between the Kordofan melon and a typical modern cultivar, 97103, and mapping the SVs in over 400 Citrullus accessions revealed shifts in allelic frequencies, suggesting that fruit sweetness has gradually increased over the course of watermelon domestication. That a likely progenitor of the watermelon still exists in Sudan has implications for targeted modern breeding efforts.

Automated summary

Wild relatives or progenitors of crops are important resources for breeding and understanding domestication, but identifying them is challenging due to extinction, hybridization, and the difficulty of distinguishing them from feral forms. This study used collection-based systematics, iconography, and resequenced accessions to find the potential progenitor of the domesticated watermelon, identifying a Sudanese form known as the Kordofan melon as the closest relative. Genomic analysis showed that genetic changes related to bitterness loss and fruit flesh color occurred from the progenitor to the domesticated watermelon, with fruit sweetness gradually increasing over the course of watermelon domestication.