doi: 10.1038/s41467-017-00336-7.
Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement
Naibin Duan 1 2, Yang Bai 3, Honghe Sun 4, Nan Wang 1, Yumin Ma 2, Mingjun Li 5, Xin Wang 4, Chen Jiao 4, Noah Legall 4, Linyong Mao 4, Sibao Wan 6, Kun Wang 7, Tianming He 8, Shouqian Feng 1, Zongying Zhang 1, Zhiquan Mao 1, Xiang Shen 1, Xiaoliu Chen 1, Yuanmao Jiang 1, Shujing Wu 1, Chengmiao Yin 1, Shunfeng Ge 1, Long Yang 1, Shenghui Jiang 1, Haifeng Xu 1, Jingxuan Liu 1, Deyun Wang 1, Changzhi Qu 1, Yicheng Wang 1, Weifang Zuo 1, Li Xiang 1, Chang Liu 9, Daoyuan Zhang 10, Yuan Gao 7, Yimin Xu 4, Kenong Xu 6, Thomas Chao 11, Gennaro Fazio 11, Huairui Shu 1, Gan-Yuan Zhong 11, Lailiang Cheng 6, Zhangjun Fei 12 13, Xuesen Chen 14
Affiliations
- PMID:28811498
- PMCID: PMC5557836
- DOI: 10.1038/s41467-017-00336-7
Item in Clipboard
Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement
Naibin Duan et al. Nat Commun..
Display options
Format
Display options
Format
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.
Conflict of interest statement
The authors declare no competing financial interests.
Figures
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, withred squares representing rootstocks andred 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. Eachvertical bar represents one apple accession and thex axis shows different apple accessions. Eachcolor represents one putative ancestral background and they axis quantifies ancestry membership. AsiM. asiatica, BacM. baccata, DomM. domestica, HupM. hupehensis,Other other wild species, RobM. robusta, Sie_KM. sieversii in Kazakhstan, Sie_XM. sieversii in Xinjiang, SylM. sylvestris
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 (r2) by pairwise physical distance inM. domestica,M. sieversii in Kazakhstan,M. sieversii in Xinjiang,M. sylvestris, and other wild species.c Multidimensional scaling (MDS) plot for the pairwiseFST matrix. The Euclidean distances between each pair of groups significantly represent the correspondingFST values (Spearman rank-sum correlationρ = 0.95;p < 10−14).d Major alleles of scion and rootstock cultivars derived fromM. sieversii in Kazakhstan andM. sylvestris. AsiM. asiatica, BacM. baccata, DomM. domestica, HupM. hupehensis, RobM. robusta, Sie_KM. sieversii in Kazakhstan, Sie_XM. sieversii in Xinjiang, SylM. sylvestris
Genome-wide distribution of selective sweeps inM. domestica.a Selective sweeps inM. domestica compared withM. sieversii in Kazakhstan.b Selective sweeps inM. domestica compared withM. 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, andblue boxes represent local GO enriched regions with associated traits labeled below. Selective regions shared by both comparisons are shaded withlight blue bars, while interesting regions only identified in one of the two comparisons are shaded withlight 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
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 QTLsfw1 andfw2, distributions of XP-CLR scores are shown. Selective sweeps are marked withred bars and interesting genes are labeled above peaks.bMiRNA172g/miRNA172h and the two target genes that contain highly divergent SNPs (pointed byarrows) betweenM. 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
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) inM. domestica fromM. sieversii in Kazakhstan (Dom_SieK) and chromosome 12 (c) fromM. sylvestris (Dom_syl), which harbor genes known to be associated with fruit firmness. Distributions of XP-CLR scores are shown intop panels with selective sweeps marked withred bars and interesting genes labeled above peaks. Distributions of π are shown inbottom panels withM. domestica inorange lines, andM. sieversii andM. sylvestris ingreen 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
Domestication of fruit sweetness and acidity in apples.a Selective sweeps fromM. sieversii in Kazakhstan that co-localize with a sorbitol QTL.b Domestication sweeps fromM. sylvestris that contain key genes for sugar metabolism. Distributions of XP-CLR scores are shown. Selective sweeps are marked withred bars and interesting genes are labeled above peaks.c–f Domestication of theMa1 gene that regulates apple fruit acidity.c Distributions of nucleotide diversity (π) ofM. domestica (red),M. sieversii in Kazakhstan (blue), andM. sylvestris (green) in theMa1 genome region.dMa1 selective sweeps during domestication fromM. sieversii in Kazakhstan (blue) andM. sylvestris (green). Sweep regions are marked withfilled boxes.e Distribution ofFST betweenM. domestica andM. sieversii in Kazakhstan in theMa1 genome region.f Distribution ofFST betweenM. domestica andM. sylvestris in theMa1 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
References
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources
Other Literature Sources