Kiwifruits, belonging to the genus Actinidia, are acknowledged as one of the most successfully domesticated fruits in the twentieth century. Despite the rich wild resources and diverse phenotypes within this genus, insights into the genomic changes are still limited. Here, we conducted whole-genome sequencing on seven representative materials from highly diversified sections of Actinidia, leading to the assembly and annotation of 14 haplotype genomes with sizes spanning from 602.0 to 699.6 Mb. By compiling these haplotype genomes, we constructed a super pan-genome for the genus. We identified numerous structural variations (SVs, including variations in gene copy number) and highly diverged regions in these genomes. Notably, significant SV variability was observed within the intronic regions of the MED25 and TTG1 genes across different materials, suggesting their potential roles in influencing fruit size and trichome formation. Intriguingly, our findings indicated a high genetic divergence between two haplotype genomes, with one individual, tentatively named Actinidia × leiocacarpae, from sect. Leiocacarpae. This likely hybrid with a heterozygous genome exhibited notable genetic adaptations related to resistance against bacterial canker, particularly through the upregulation of the RPM1 gene, which contains a specific SV, after infection by Pseudomonas syringae pv. actinidiae. In addition, we also discussed the interlineage hybridizations and taxonomic treatments of the genus Actinidia. Overall, the comprehensive pan-genome constructed here, along with our findings, lays a foundation for examining genetic compositions and markers, particularly those related to SVs, to facilitate hybrid breeding aimed at developing desired phenotypes in kiwifruits.

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