Sapindus mukorossi is an environmentally friendly plant and renewable energy source whose fruit has been widely used for biomedicine, biodiesel, and biological chemicals due to its richness in saponin and oil contents. Here, we report the first chromosome-scale genome assembly of S. mukorossi (covering ~391 Mb with a scaffold N50 of 24.66 Mb) and characterize its genetic architecture and evolution by resequencing 104 S. mukorossi accessions. Population genetic analyses showed that genetic diversity in the southwestern distribution area was relatively higher than that in the northeastern distribution area. Gene flow events indicated that southwest species may be the donor population for the distribution areas in China. Genome-wide selective sweep analysis showed that a large number of genes are involved in defense responses, growth and development, including SmRPS2, SmRPS4, SmRPS7, SmNAC2, SmNAC23, SmNAC102, SmWRKY6, SmWRKY26, and SmWRKY33. We also identified several candidate genes controlling six agronomic traits by genome-wide association studies, including SmPCBP2, SmbHLH1, SmCSLD1, SmPP2C, SmLRR-RKs, and SmAHP. Our study not only provides a rich genomic resource for further basic research on Sapindaceae woody trees but also identifies several economically significant genes for genomics-enabled improvements in molecular breeding.

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