Whole-genome sequencing revealed the genomic origin of Solanum demissum Lindl., a Mexican hexaploid wild potato species

BACKGROUND: Solanum demissum Lindl. (2n = 6x = 72) is the most popular wild species in potato breeding because of its resistance to late blight, caused by Phytophthora infestans (Mont.) de Bary. Regular meiosis with 36 bivalents indicates that S. demissum has three distinct genomes, but their origin remains unknown. RESULTS: We constructed a chromosome-scale assembly of S. demissum using PacBio long-read sequencing and Hi-C scaffolding technologies. The final assembly comprised 2.035 Gb anchored to 36 chromosome-level scaffolds, which were phased into three subgenomes (SG1, SG2, and SG3, with sizes of 696.51 Mb, 685.32 Mb, and 653.29 Mb, respectively). Evidence-based annotation, using RNA-seq datasets, and deep learning-based prediction identified 32,888 genes in SG1, 33,028 in SG2, and 31,999 in SG3. Comparing gene sequences among the three subgenomes and 47 other genomes from diverse collections distinctly placed these subgenomes in the phylogenetic tree; the most closely related were SG1 with the maternal and A-genome ancestor S. verrucosum, SG2 with SG2 of S. acaule, and SG3 with SG1 of S. acaule. Syntenic ratios, indicating genome structure similarity, further supported these relationships. The three subgenomes of S. demissum exhibited mostly balanced gene expression. Additionally, the composition and genome occupancy of transposable elements, as well as the number of resistance genes, are similar across the three subgenomes and more closely resemble those of the ancestral genomes in S. acaule and S. verrucosum. CONCLUSIONS: Solanum demissum likely originated between a Mexican diploid S. verrucosum as the female parent and a South American tetraploid S. acaule as the male parent.