Genome-wide view of genetic diversity reveals paths of selection and cultivar differentiation in peach domestication

Abstract

Domestication and cultivar differentiation are requisite processes for establishing cultivated crops. These processes inherently involve substantial changes in population structure, including those from artificial selection of key genes. In this study, accessions of peach (Prunus persica) and its wild relatives were analysed genome-wide to identify changes in genetic structures and gene selections associated with their differentiation. Analysis of genome-wide informative single-nucleotide polymorphism loci revealed distinct changes in genetic structures and delineations among domesticated peach and its wild relatives and among peach landraces and modern fruit (F) and modern ornamental (O-A) cultivars. Indications of distinct changes in linkage disequilibrium extension/decay and of strong population bottlenecks or inbreeding were identified. Site frequency spectrum- and extended haplotype homozygosity-based evaluation of genome-wide genetic diversities supported selective sweeps distinguishing the domesticated peach from its wild relatives and each F/O-A cluster from the landrace clusters. The regions with strong selective sweeps harboured promising candidates for genes subjected to selection. Further sequence-based evaluation further defined the candidates and revealed their characteristics. All results suggest opportunities for identifying critical genes associated with each differentiation by analysing genome-wide genetic diversity in currently established populations. This approach obviates the special development of genetic populations, which is particularly difficult for long-lived tree crops.

Keywords: artificial selection; cultivar differentiation; domestication; linkage disequilibrium; tree crop.

Figure 1.

Evolutionary tree of domesticated peach and its wild relatives. Evolutionary tree constructed by a maximum likelihood (ML) approach using information from 5,180 genome-wide SNPs in 87 accessions of domesticated peach (Prunus persica) and five wild species (P. davidiana, P. mira, P. kansuensis, P. tangutica, and P. webbii), with 8 accessions of outgroup species (P. salicina, P. mume, and P. avium). Operational taxonomic units (OTU) are colored in ocher, black, green, blue, and red, for major clusters: wild species (W), landraces (L) (EA and OT for accessions in East Asia and other region, respectively), modern fruit cultivars (F), and modern ornamental cultivars (O-A and O-B for only ornamental usage, and FO for fruit and ornamentals), respectively, according to the tree topology, and to classical classifications considering uses and morphologies. The main differentiation steps of the domesticated peach, the East Asian cultivars (including modern cultivars), the O-A cluster, and the F cluster, are shown as black, green, red, and blue thick branches, respectively, with statistically significant support (bootstrap > 650/1,000, except for the differentiation to the East Asian cultivars).

Figure 2.

Population structure analysis in peach. (A) Principal component analysis using information from 5,180 genome-wide SNPs in 87 accessions including domesticated peach and its wild relatives (right) and in 67 accessions focusing on domesticated peach (left). The first two components in PCA (PC1 and PC2) are plotted on the axes to visualize the genetic relationships. The proportion of variance explained by each PC is given in parentheses along each axis. The wild species is shown as a cross. The landraces are shown as squares in green and yellow for accessions in East Asia and other regions, respectively. The modern cultivars are shown as circles in blue and red, corresponding to fruit and ornamental cultivars, respectively. (B and C) Structure analysis of subdivision of the population (K = 2–7), with STRUCTURE 2.2 (B) and with InStruct (C). Each individual is shown as a vertical bar. In K = 2, wild species showed a cluster distinct from domesticated peach, except for two accessions experiencing frequent hybridization with domesticated peach. In K = 5 or more, the F, L-OT, and O-A/O-B/L-EA clusters show clear separation. The O-A and O-B/L-EA showed significant separation at K = 7 or more.

Figure 3.

Comparison of LD decay in the wild species and each variety complex of domesticated peach. The average values of R² in pairwise LD among the 1,346 SNPs on Chromosome 4, which carries the most SNPs among the eight chromosomes, in windows of up to 10,000 kb are shown. The Y-axis standards are adjusted according to the background values in each subpopulation for visualization of LD decay for comparison among subpopulations. The X-axis shows physical distance among the SNPs, and the average R² values at 100-kb intervals are plotted. (A) Comparison of LD decay in domesticated peach and wild relatives. Black and white arrows indicate LD decay points in domesticated peach and wild relative, respectively. (B) Comparison of LD decay in the F, O-A, L-EA, and L-OT clusters. The F cluster shows only significantly expanded LD, as shown by the black arrow, in comparison to the other clusters, whose LD decays are shown with white arrows and black bars.

Figure 4.

Genome-wide selective sweep analysis based on ZH_p, in the domesticated peach and two modern varietal complexes. (A) Transitions of Z-transformed values of H_p in 400-kb bins with 100-kb steps are shown for the domesticated peach population and two subpopulations, the F and O-A clusters. Putative regions showing selective sweeps (P < 0.001) are indicated by outlined triangles. (B) For the F and O-A clusters, plots of relative values of H_p in 400-kb bins with 100-kb steps against the L cluster are shown. Putative regions showing selective sweeps in the paths of differentiation from landraces are indicated by triangles. For the two regions indicated by black triangles, detailed characterization of ZH_p in a comparison among four subpopulations (F, O-A, L-EA, and L-OT) is shown in (C) for the top of Chromosome 7, which corresponded to a putative selective sweep in the F cluster, and in (D) for the bottom of Chromosome 4, showing a putative selective sweep in the O-A cluster.

Figure 5.

Genome-wide analysis for positive selection based on EHH. (A) iHS from each SNP core showing heterozygous states in one population transformed to P values with R and plotted as a logarithmic value. Underlining indicates threshold values for selection (P < 0.0001). (B) XP-EHH from each SNP core showing the same nucleotide between the subject and the comparison target, also transformed to P values and plotted in logarithmic scale. For the domesticated peach, the wild relative cluster was used for comparison. For the F and O-A clusters, the landrace (L) cluster was independently used for comparison. Underlining indicates threshold values for selection (P < 0.001). In both iHS and XP-EHH tests, putative selected regions are indicated by outlined triangles.