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• First high-quality, chromosome-scale genome assembly and first complete chloroplast genome of water spinach. • Water spinach and the lineage (Ipomoea nil, I. trifida and I. triloba) diverged around 7.1 million years ago. • Synteny analysis revealed obvious one-to-one collinearity for all 15 pseudo-chromosomes between the genomes of water spinach and I. triloba , with small-scale interchromosomal rearrangements. • Species-specific genome expansion of Gypsy in water spinach. • Heavy metal associated genes were expanded in the water spinach genome. Water spinach (Ipomoea aquatica) is one of the most popular green leafy vegetables in Asia, with both aquatic and terrestrial characteristics. We report here its high-quality, chromosome-scale genome assembly through a combination of PacBio sequencing, short-read sequencing, 10 × Genomics and a high-density genetic map. This assembly contains 1,392 scaffolds (N50 = 2.75 Mb) covering 93.3% of the estimated genome (550.03 Mb). Of the assembly, 90% was anchored to 15 pseudo-chromosomes containing 162 scaffolds (415.77 Mb). We also assembled a complete chloroplast genome of 165, 294 bp with 111 genes, encoding 84 proteins, 8 rRNA, and 19 tRNA. This species includes 30, 693 predicted protein-coding genes. By clustering results of the genomes, there are 3,431 gene families specific to the four Ipomoea species and 34 gene families in common of O. sativa, U. gibba and I. aquatica. These genes from the 34 gene familes may be related to the aquatic characteristics of plants. Phylogenetic analysis reveals that I. aquatica and the lineage (I. nil, I. trifida and I. triloba) diverged around 7.1 million years ago. Synteny analysis revealed obvious one-to-one collinearity for all 15 pseudo-chromosomes between the genomes of water spinach and I. triloba , with small-scale interchromosomal rearrangements. Compared with Copia, there are more Gypsies in the genome of water spinach suggesting species-specific genome expansion of Gypsy in water spinach. The 4DTv analysis confirmed the WGD event in the ancestor of the Ipomoea lineage and Cuscuta lineage. Transcriptome analysis reveals that there are 23,828 genes co-expressed in roots, flowers, leaves and stems. We also found that heavy metal associated genes were expanded in the genome. The genome sequence is a valuable resource for functional genomics and the genome assisted breeding of water spinach. [ABSTRACT FROM AUTHOR]