Diversification and independent domestication of Asian and European pears

Abstract

Background: Pear (Pyrus) is a globally grown fruit, with thousands of cultivars in five domesticated species and dozens of wild species. However, little is known about the evolutionary history of these pear species and what has contributed to the distinct phenotypic traits between Asian pears and European pears.

Results: We report the genome resequencing of 113 pear accessions from worldwide collections, representing both cultivated and wild pear species. Based on 18,302,883 identified SNPs, we conduct phylogenetics, population structure, gene flow, and selective sweep analyses. Furthermore, we propose a model for the divergence, dissemination, and independent domestication of Asian and European pears in which pear, after originating in southwest China and then being disseminated throughout central Asia, has eventually spread to western Asia, and then on to Europe. We find evidence for rapid evolution and balancing selection for S-RNase genes that have contributed to the maintenance of self-incompatibility, thus promoting outcrossing and accounting for pear genome diversity across the Eurasian continent. In addition, separate selective sweep signatures between Asian pears and European pears, combined with co-localized QTLs and differentially expressed genes, underline distinct phenotypic fruit traits, including flesh texture, sugar, acidity, aroma, and stone cells.

Conclusions: This study provides further clarification of the evolutionary history of pear along with independent domestication of Asian and European pears. Furthermore, it provides substantive and valuable genomic resources that will significantly advance pear improvement and molecular breeding efforts.

Keywords: Fruit-related traits; Independent domestication; Origin and evolution; Pear (Pyrus); Re-sequencing genomes; Self-incompatibility.

Fig. 1

PCA and LD analysis of 113 cultivated and wild pear accessions based on whole-genome SNP analysis. a PCA plots of the first two eigenvectors of all 113 pear accessions. b LD decay determined by correlation of allele frequencies (r²) against distance (kb) among polymorphic SNP sites in different pear groups, including cultivated Asian (red), cultivated European (light blue), wild Asian (blue), and wild European (green)

Fig. 2

Phylogenetic tree and gene flow analysis. a Phylogenetic tree and the population structure (K = 5) of all 113 pear accessions inferred from whole-genome SNPs, with apple (Malus× domestica) used as an outgroup. Each color corresponds to a single population as noted. In population structure, each accession is represented by a horizontal bar. Pyw and Pyc indicate wild and cultivated accessions, respectively, and other codes correspond to abbreviated names of pear species. b Population structure (K = 2) of European pears. c Detection of gene flow within Asian pears. d Detection of gene flow within European pears; subgroup 1 and subgroup 2. e Detection of gene flow between Asian and European pears. Lines represent gene flow; arrows indicate the direction of gene flow. The scale bar shows a tenfold average standard error of the entries in the sample covariance matrix. The color bar shows the migration weight: a red color denotes a strong gene flow, while a yellow color denotes a weak gene flow. f IBD analysis exploring the genetic background of P. sinkiangensis from a combination of Asian and European pears. Blocks originating from Asian and European pears were identified in P. sinkiangensis Pyc-si1

Fig. 3

Genetic relationships of wild pears in different geographical regions. a Wild pear distribution in different geographical regions. b Population structure (K = 3) of all 57 wild accessions. Each color corresponds to a single population as noted. Each accession is represented by a vertical bar. Different color represents the probability of an accession belonging to a different genetic background. c PCA plots of wild accessions. d Phylogenetic tree of wild pear accessions and admixed genetic component of some species. e Distribution of F_ST values between three major wild groups. f ϴπ values of different pear groups. Asian group II, wild accessions distributed in south and west regions of China; Asian group III, wild accessions distributed in the northeast region of China. European group I was split into three subgroups: Central Asia, West Asia, and the European mainland. g Lineage homologies of wild accessions of both Asian and European pears by identity-by-descent (IBD)

Fig. 4

Genetic relationships and divergence times of pear species. a Genetic relationships of wild and cultivated pear species. b Divergence time of Asian and European pears. A, Vitis vinifera; B, Malus × domestica; C, Pyrus communis; D, Pyrus bretschneideri; E, Prunus persica; F, Fragaria vesca; G, Populus trichocarpa; H, Carica papaya; and I, Arabidopsis thaliana

Fig. 5

Distinct domestication signals in Asian and European pears. a Distribution of F_ST values across the whole genome of Asian pears. b Distribution of F_ST values across the whole genome of European pears. c Distribution of ROD values across the whole genome of Asian pears. d Distribution of ROD values across the whole genome of European pears. Yellow arrows indicate genes in selective sweeps of only Asian pears. Purple arrows indicate genes in selective sweeps of only European pears. Red arrows indicate genes in selective sweeps common to both the Asian and European pears. The horizontal dotted line indicates the threshold of F_ST 5% and ROD > 0.5, respectively. e Overlap of selective sweeps and QTLs related to fruit traits in pear. The inside lines of each linkage group indicate selective sweeps, while the outside lines of each linkage group indicate QTLs. A total of 208 selective sweeps in Asian pears showed coincidence with QTLs related to fruit traits, including sugar, acidity, stone cell, firmness, fruit size, fruit shape, as well as traits for preharvest fruit drop and fruit harvest time. A total of 14 selective sweeps in European pears showed coincidence with QTLs related to fruit traits, including sugar, acidity, firmness, fruit size, fruit shape, and skin color

Fig. 6

Sugar metabolism-related genes associated with domestication of pear. Genes in red correspond to genes in selective sweep regions. Transcriptome data are derived from wild and cultivated pear fruits. The two wild pears are ‘Baitanggengzi’ and ‘Tiantanggengzi’ (from left to right), while the four cultivated pears are ‘Yali’, ‘Hosui’, ‘Nanguo’, and ‘Starkrimson’ (from left to right). FK fructokinase, PFK phosphofructokinase, FBA fructose-bisphosphate aldolase, INV beta-fructofuranosidase, EG endoglucanase, TPP trehalose-phosphatase, STS stachyose synthetase, β-GAL beta-galactosidase, α-GLU alpha-glucosidase, SS starch synthase, SOT sorbitol transporter, HT hexose transporter