Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement

Abstract

Human selection has reshaped crop genomes. Here we report an apple genome variation map generated through genome sequencing of 117 diverse accessions. A comprehensive model of apple speciation and domestication along the Silk Road is proposed based on evidence from diverse genomic analyses. Cultivated apples likely originate from Malus sieversii in Kazakhstan, followed by intensive introgressions from M. sylvestris. M. sieversii in Xinjiang of China turns out to be an "ancient" isolated ecotype not directly contributing to apple domestication. We have identified selective sweeps underlying quantitative trait loci/genes of important fruit quality traits including fruit texture and flavor, and provide evidences supporting a model of apple fruit size evolution comprising two major events with one occurring prior to domestication and the other during domestication. This study outlines the genetic basis of apple domestication and evolution, and provides valuable information for facilitating marker-assisted breeding and apple improvement.Apple is one of the most important fruit crops. Here, the authors perform deep genome resequencing of 117 diverse accessions and reveal comprehensive models of apple origin, speciation, domestication, and fruit size evolution as well as candidate genes associated with important agronomic traits.

Fig. 1

Population structure of 117 domesticated and wild apples. a Neighbor-joining phylogenetic tree constructed using SNPs at fourfold degenerate sites. Each species group is color coded, with red squares representing rootstocks and red dots scions. b Principal component analysis (PCA) of the 117 apple accessions. c Bayesian model-based clustering of the 117 apple accessions with the number of ancestry kinship (K) from 3 to 5. Each vertical bar represents one apple accession and the x axis shows different apple accessions. Each color represents one putative ancestral background and the y axis quantifies ancestry membership. Asi M. asiatica, Bac M. baccata, Dom M. domestica, Hup M. hupehensis, Other other wild species, Rob M. robusta, Sie_K M. sieversii in Kazakhstan, Sie_X M. sieversii in Xinjiang, Syl M. sylvestris

Fig. 2

Apple evolutionary map. a Apple evolutionary map along the west and east bounds of the Silk Route with center of origin at Kazakhstan in central Asia. b Decay of linkage disequilibrium (LD) measured as the squared correlation coefficient (r ²) by pairwise physical distance in M. domestica, M. sieversii in Kazakhstan, M. sieversii in Xinjiang, M. sylvestris, and other wild species. c Multidimensional scaling (MDS) plot for the pairwise F _ST matrix. The Euclidean distances between each pair of groups significantly represent the corresponding F _ST values (Spearman rank-sum correlation ρ = 0.95; p < 10⁻¹⁴). d Major alleles of scion and rootstock cultivars derived from M. sieversii in Kazakhstan and M. sylvestris. Asi M. asiatica, Bac M. baccata, Dom M. domestica, Hup M. hupehensis, Rob M. robusta, Sie_K M. sieversii in Kazakhstan, Sie_X M. sieversii in Xinjiang, Syl M. sylvestris

Fig. 3

Genome-wide distribution of selective sweeps in M. domestica. a Selective sweeps in M. domestica compared with M. sieversii in Kazakhstan. b Selective sweeps in M. domestica compared with M. sylvestris. XP-CLR scores are plotted across the 17 chromosomes in the apple genome with key functional enzyme genes labeled above the dot peaks. Red vertical boxes illustrate selective sweeps, and blue boxes represent local GO enriched regions with associated traits labeled below. Selective regions shared by both comparisons are shaded with light blue bars, while interesting regions only identified in one of the two comparisons are shaded with light yellow bars. Traits include fruit acidity (A), color (C), firmness (F), hormone (H), soluble sugar (S), and secondary metabolites (M). Gene abbreviations: ALMT aluminum-activated malate transporter, ACO 1-aminocyclopropane-1-carboxylate oxidase, ACS 1-aminocyclopropane-1-carboxylate synthase, AE aldose 1-epimerase, AR aldose reductase, BG beta-galactosidase, CAS cycloartenol synthase, CTS citrate synthase, CLS cellulose synthase, FH flavanone 3-hydroxylase, GA3OX gibberellin 3-beta-dioxygenase, GG glucan endo-1,3-b-glucosidase, GMD GDP-mannose 4,6-dehydratase, IFR isoflavone reductase, IMS, 2-isopropylmalate synthase, MD malate dehydrogenase, PDC pyruvate decarboxylase, PDK pyruvate dehydrogenase kinase, PE pectin esterase, PFK 6-phospho-fructokinase, PG polygalacturonase, PL pectate lyase, SPD sorbitol 6-phosphate dehydrogenase, SPS sucrose phosphate synthase, SS sucrose synthase, ST sugar transporter

Fig. 4

Evolution of fruit size during speciation and domestication in apple. a Domestication sweeps underlying apple fruit size QTLs. Within the physical intervals (orange boxes) of the two fruit weight QTLs fw1 and fw2, distributions of XP-CLR scores are shown. Selective sweeps are marked with red bars and interesting genes are labeled above peaks. b MiRNA172g/miRNA172h and the two target genes that contain highly divergent SNPs (pointed by arrows) between M. domestica with large fruits and other wild species bearing very small fruits. c Schematic diagram of the two-step evolution of apple fruit size. BG beta-galactosidase, FBP fructose-1,6-bisphosphatase, FD ferredoxin, PPD pyruvate phosphate dikinase, P4 patellin-4, UGE UDP-glucose 4-epimerase

Fig. 5

Domestication sweeps underlying apple fruit firmness. Distributions of XP-CLR scores and nucleotide diversity (π) in selective regions on chromosomes 6 (a) and 17 (b) in M. domestica from M. sieversii in Kazakhstan (Dom_SieK) and chromosome 12 (c) from M. sylvestris (Dom_syl), which harbor genes known to be associated with fruit firmness. Distributions of XP-CLR scores are shown in top panels with selective sweeps marked with red bars and interesting genes labeled above peaks. Distributions of π are shown in bottom panels with M. domestica in orange lines, and M. sieversii and M. sylvestris in green lines. AE aldose 1-epimerase, CLS cellulose synthase, GG glucan endo-1,3-b-glucosidase, MM endo-beta-1,4-mannase, PE pectinesterase, PG polygalacturonase, PL pectate lyase

Fig. 6

Domestication of fruit sweetness and acidity in apples. a Selective sweeps from M. sieversii in Kazakhstan that co-localize with a sorbitol QTL. b Domestication sweeps from M. sylvestris that contain key genes for sugar metabolism. Distributions of XP-CLR scores are shown. Selective sweeps are marked with red bars and interesting genes are labeled above peaks. c–f Domestication of the Ma1 gene that regulates apple fruit acidity. c Distributions of nucleotide diversity (π) of M. domestica (red), M. sieversii in Kazakhstan (blue), and M. sylvestris (green) in the Ma1 genome region. d Ma1 selective sweeps during domestication from M. sieversii in Kazakhstan (blue) and M. sylvestris (green). Sweep regions are marked with filled boxes. e Distribution of F _ST between M. domestica and M. sieversii in Kazakhstan in the Ma1 genome region. f Distribution of F _ST between M. domestica and M. sylvestris in the Ma1 genome region. bHLH transcription factor, CTS citrate synthase, HK hexokinase, MYB transcription factor, PDK pyruvate dehydrogenase kinase, PE pectin esterase, PG polygalacturonase, PK pyruvate kinase, SBT sorbitol transporter, SS sucrose synthase, ST sugar transporter