Genomic evidence for evolutionary history and local adaptation of two endemic apricots: Prunus hongpingensis and P. zhengheensis

Abstract

Apricot, belonging to the Armeniaca section of Rosaceae, is one of the economically important crop fruits that has been extensively cultivated. The natural wild apricots offer valuable genetic resources for crop improvement. However, some of them are endemic, with small populations, and are even at risk of extinction. In this study we unveil chromosome-level genome assemblies for two southern China endemic apricots, Prunus hongpingensis (PHP) and P. zhengheensis (PZH). We also characterize their evolutionary history and the genomic basis of their local adaptation using whole-genome resequencing data. Our findings reveal that PHP and PZH are closely related to Prunus armeniaca and form a distinct lineage. Both species experienced a decline in effective population size following the Last Glacial Maximum (LGM), which likely contributed to their current small population sizes. Despite the observed decrease in genetic diversity and heterozygosity, we do not observe an increased accumulation of deleterious mutations in these two endemic apricots. This is likely due to the combined effects of a low inbreeding coefficient and strong purifying selection. Furthermore, we identify a set of genes that have undergone positive selection and are associated with local environmental adaptation in PHP and PZH, respectively. These candidate genes can serve as valuable genetic resources for targeted breeding and improvement of cultivated apricots. Overall, our study not only enriches our comprehension of the evolutionary history of apricot species but also offers crucial insights for the conservation and future breeding of other endemic species amidst rapid climate changes.

Figure 1

Distribution and morphological characters of Armeniaca section species. A Geographic distribution of apricot species used in this study. Different color ranges in the map indicate the distribution of individuals in each population. B Photographs of leaves, fruit, and fruit stone of PHP, PZH, P. armeniaca, and mei. Scale bar = 1 cm.

Figure 2

Genomic features and evolution of PHP and PZH. A Circos display of genomic features of PHP and PZH. The Circos tracks represent (a) chromosome ideogram (Mb scale), (b) gene density (slide window = 100 kb, overlap = 0 kb), (c) repeat density (slide window = 100 kb, overlap = 0 kb), (d) LTR-Gypsy density (slide window = 100 kb, overlap = 0 kb), (e) LTR-Copia density (slide window = 100 kb, overlap = 0 kb), (f) genome synteny among PHP, PZH, and P. armeniaca (synteny block length >5 kb). B Divergence time tree estimated using the MCMCtree of the PAML package. Numbers on the nodes are median age estimates and 95% highest posterior densities (Mya). Fossil calibration points are indicated by orange stars. Expansion and contraction gene families are presented under each species. C Synonymous substitution rate (K_s) density distributions of intraspecies synteny of PHP, PZH, P. armeniaca, and mei. D Length of SVs detected between the genomes of PHP and P. armeniaca and the genomes of PZH and P. armeniaca. E Structural variation between the genomes of PHP and P. armeniaca and the genomes of PHP and P. armeniaca, including synteny, inversions, translocations, and duplications.

Figure 3

Population delimitation of five apricot species. A A maximum likelihood phylogenetic tree was constructed by IQ-TREE with an ascertainment bias correction (+ASC) model and visualized by FigTree. All the bootstrap values are 100 along the branches. B Population structure by ADMIXTURE analysis for the optimal K = 4 and 5. Each color-coded bar corresponds to an individual, and the segmented colors illustrate the proportions of ancestral components. C PCA based on genomic SNPs of all accessions. D PCA constructed after the removal of all P. mume individuals. The colors in (C) and (D) correspond to those in (A). E Pairwise population differentiation was estimated using F_ST. F Decay of LD was calculated based on r² of all apricot accessions.

Figure 4

Divergence and demographic histories of the different apricot populations. A Population divergence times based on a SNAPP analysis. The estimated divergence times at specific nodes were guided by a singular calibration, denoted by an star. Median age estimates, accompanied by 95% HPDs (Mya), have been provided for each respective node. B Comparison of historical effective population size (N_e) changes across the various populations.

Figure 5

Assessment of heterozygosity, inbreeding level, and deleterious variants. A Expected heterozygosity (H_e) and inbreeding coefficient (F_IS) of all populations, excluding mei. C, D Ratio of derived deleterious (C) and LOF (D) variants to synonymous variants in homozygous (circle) and heterozygous (square) tracts per individual. The ratio differences between homozygous and heterozygous tracts were calculated using the Wilcoxon rank-sum test (**P < .01; ***P < .001).

Figure 6

Gene flow analysis using various methods. A TreeMix topologies with one suggested gene flow event between the Mei, NE_Psib, NW_CA clade, PZH, and PHP populations. B Gene flow identification between PHP and CA_NW clade. We divided the CA_NW clade into CA_N_Par, CA_S_Par, and NW_Psib and then performed TreeMix analysis with one suggested gene flow event (orange arrow). C The suggested gene flow event in (A) was further evaluated using a four-taxon test. D, E Population genetic model comparison results between population sets PHP and NW_CA (D), and PZH and NW_CA (E). F Distribution of modified f_d statistics (PHP and NW_CA) and genetic diversity of selective sweeps in the 100-kb non-overlapping window. The red dashed lines indicate the threshold (5%) of modified f_d statistics and π. The light gray range indicates the low π and f_d values, and dark gray indicates the high π and f_d values. G GO enrichment analysis of 756 genes with the modified f_d value higher than the top 5%.

Figure 7

Selection signatures in the genomes of PHP and PZH under local adaptation. A PCA for environmental variables of five apricot species (seven populations). The percentages of variation explained by each principal component are indicated in parentheses. Elev, elevation; bio1, annual mean temperature; bio5, maximum temperature of warmest month; bio6, minimum temperature of coldest month; bio7, annual temperature range (bio5 − bio6); bio12, annual precipitation; bio13, precipitation of wettest month; bio14, precipitation of driest month; bio15, precipitation seasonality (coefficient of variation). B Manhattan plot of CLR of PHP and PZH. The dashed line indicates the CLR value threshold (top 5%). Functionally characterized candidate genes are denoted (Supplementary Data Tables S12 and S13). Venn diagram of the top 5% genes of PHP and PZH. C Tajima’s D statistic and XP-EHH test for the top 5% and bottom 95% genes in CLR analysis. Asterisks indicate the degree of significance in both the Wilcoxon rank-sum test and the t-test (***P < 0.001). D Signals of artificial selection in BAS1 and GolS2 genes in PHP and DJC1 and CRL1 genes in PZH.