High‐quality chromosome‐level genomes of Cucumis metuliferus and Cucumis melo provide insight into Cucumis genome evolution

• Published in: The Plant journal : for cell and molecular biology 2021-07, Vol.107 (1), p.136-148
• Main Authors: Ling, Jian, Xie, Xiaoxiao, Gu, Xingfang, Zhao, Jianlong, Ping, Xingxing, Li, Yan, Yang, Yuhong, Mao, Zhenchuan, Xie, Bingyan
• Format: Article
• Language: English
• Subjects: Binding sites; Chromosome translocations; Chromosomes; Crop improvement; Cucumbers; Cucumis; Cucumis melo; Cucumis metuliferus; cucurbit; Cucurbitaceae; Divergence; Evolution; Evolutionary genetics; Fruits; Genes; genome evolution; Genomes; Inversions; Leucine; Molecular evolution; NBS-LRR gene; Nematodes; Nucleotide sequence; Nucleotides; Pest resistance; Phylogeny; Population structure; resistance‐related gene; Structural analysis; variation map; Viruses
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.15279

Summary Cucumis metuliferus (African horned cucumber), a wild relative of Cucumis sativus (cucumber) and Cucumis melo (melon), displays high‐level resistance to several important plant pathogens (e.g., root‐knot nematodes and several viruses). Here, we report a chromosome‐level genome assembly for C. metuliferus, with a 316 Mb genome sequence comprising 29 039 genes. Phylogenetic analysis of related species in family Cucurbitaceae indicated that the divergence time between C. metuliferus and melon was 17.8 million years ago. Comparisons between the C. metuliferus and melon genomes revealed large structural variations (inversions and translocations >1 Mb) in eight chromosomes of these two species. Gene family comparison showed that C. metuliferus has the largest number of resistance‐related nucleotide‐binding site leucine‐rich repeat (NBS‐LRR) genes in Cucurbitaceae. The loss of NBS‐LRR loci caused by large insertions or deletions (indels) and pseudogenization caused by small indels explained the loss of NBS‐LRR genes in Cucurbitaceae. Population structure analysis suggested that C. metuliferus originated in Zimbabwe, then spread to other southern African regions where it likely underwent similar domestic selection as melon. This C. metuliferus reference sequence will accelerate the understanding of the molecular evolution of resistance‐related genes and enhance cucurbit crop improvement efforts. Significance Statement The chromosome‐level genome of Cucumis metuliferus was reported, and the population sequencing revealed the origin and evolution of C. metuliferus. This study displayed the genome evolution among Cucumis and revealed the evolution pattern of nucleotide‐binding site leucine‐rich repeat genes in Cucurbitaceae.