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. 2022 Jan 5:9:uhac012.
doi: 10.1093/hr/uhac012.

Chromosome-scale assembly and population diversity analyses provide insights into the evolution of Sapindus mukorossi

Ting Xue  1   2 , Duo Chen  2 , Tianyu Zhang  3 , Youqiang Chen  2 , Huihua Fan  4 , Yunpeng Huang  4 , Quanlin Zhong  1 , Baoyin Li  1
Affiliations

Chromosome-scale assembly and population diversity analyses provide insights into the evolution of Sapindus mukorossi

Ting Xue et al. Hortic Res. .

Abstract

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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Figures

Figure 1
Figure 1
Representative photographs of S. mukorossi. a Mature S. mukorossi tree in its natural habitat. b Flowers. c, d Fruits. Bar =1 cm.
Figure 2
Figure 2
Characterization and evolution of the S. mukorossi genome. a Genome features across 14 chromosomes. (a) The 14 assembled chromosomes; (b) GC content; (c) gene density; (d) summary of gene expression in roots, stems, and leaves; (e) Transposable element density over the genome in non-overlapping windows; (f) summary of major interchromosomal syntenic relationships. Central colored lines represent syntenic blocks; block size = 3 kb. b Phylogenetic tree and evolution analysis of S. mukorossi. Red and green fonts indicate the numbers of gene families that have expanded and contracted among 21 species, respectively. Gene family expansions are indicated in green in the pie chart, while gene family contractions are indicated in red. Bars represent the 95% highest probability densities of the estimated divergence time. cKs distribution of syntenic blocks between S. mukorossi, D. longan, and A. yangbiense. d Macrosynteny analysis between S. mukorossi, D. longan, and A. yangbiense. Each line connects a pair of orthologous genes.
Figure 3
Figure 3
Phylogeny and population genetics of 104 S. mukorossi accessions. a Phylogenetic tree of 10 S. mukorossi accessions constructed based on whole-genome SNPs. b PCA plots of 104 S. mukorossi accessions. Different colors and shapes represent different subgroups and regions, respectively. c Population structure analysis of 104 S. mukorossi accessions (K = 2 or 3). The background of each putative ancestor is shown in different colors. d Genome-wide decay of LD. e Demographic history of Ne with a generation time of 5 years. Neutral mutation rate per generation (μ) = 1.25 × 10−8.
Figure 4
Figure 4
Genome-wide detection and annotation of selective sweeps in 104 S. mukorossi accessions. a Selective sweeps were identified by πGroupIII/πGroupI and FST. The red dashed line corresponds to the thresholds for very high significance in the top 5% of the highest values. b Manhattan plots of the CLRs among the Group I and Group III S. mukorossi populations. Red and blue dashed lines indicate the threshold for the top 1% and top 5% of CLR values, respectively. Genes located within the significant CLR peaks and corresponding annotations are denoted.
Figure 5
Figure 5
Manhattan plots from GWAS for important agronomic traits in 57 S. mukorossi accessions. a Oil content. b Saponin content. c Fruit weight. d Peel-to-fruit ratio. e Seed-to-fruit ratio. f Kernel-to-fruit ratio. Gene names are highlighted in black in candidate regions potentially related to six traits in S. mukorossi. Black and gray lines indicate the threshold for the top 5% and top 1% of the highest values, respectively.
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