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

Naibin Duan,Sibao Wan,Mingjun Li,Zhiquan Mao,Youqiang Xu ,Shunfeng Ge,Gennaro Fazio,Long Yang,Changzhi Qu,Xiang Shen,Chengmiao Yin,Yuanmao Jiang,Shu-Jing Wu ,Thomas C Chao ,Huairui Shu,Shenghui Jiang,Chen Jiao,Jingxuan Liu,Zongying Zhang,Deyun Wang,Weifang Zuo,Gan-Yuan Zhong,Linyong Mao,Xiaoliu Chen,Yuan Gao,Li Xiang,Yang Bai,Yicheng Wang,Honghe Sun,Kenong Xu,Shouqian Feng,Zhangjun Fei,Chang Liu,Daoyuan Zhang,Kun Wang,Haifeng Xu,Lailiang Cheng,Tengbing He ,Xin Wang,Noah Legall,Nan Wang,Yumin Ma,Xuesen Chen

doi:10.1038/s41467-017-00336-7

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.

Highlights

We identified a region around 1.5 kb upstream of Ma1 coding sequence (CDS) with substantially reduced nucleotide diversity in M. domestica compared to M. sylvestris, and another region about 750 bp downstream of Ma1 CDS when compared to M. sieversii in Kazakhstan
The population analyses reveal that modern cultivated apples originate from M. sieversii in Kazakhstan with intensive recent introgressions from M. sylvestris, while M. sieversii in Xinjiang is an isolated ecotype with a homogeneous genetic background that holds great potential for future apple improvement
Several thousand years of selection still has accumulated a considerable amount of desirable fruit traits that make apple one of the most important fruit crops worldwide

Summary

Results

A total of 117 Malus accessions from 24 species were selected for genome sequencing, including 35 M. domestica Resequencing of the 117 apple genomes generated a total of 1060 Gb high-quality cleaned sequences, with an average of 9.06 Gb per accession that represented ~12.2× of the apple genome (Supplementary Data 1). The tree showed that accessions of M. domestica and its introgression contributor M. sylvestris formed a subclade within a large mixed clade comprising M. sieversii accessions that are considered as progenitors of cultivated apples[8, 9], while accessions of other wild species position outside this domestication-related clade (Fig. 1a). A principal component analysis (PCA) illustrated a similar pattern to the phylogenetic tree in that M. domestica, M. sieversii, and M. sylvestris accessions formed closely related clusters that were clearly separated from the dispersed accessions of other wild species (Fig. 1b). To further understand the evolutionary history of apple, we used a Bayesian clustering algorithm with admixed models[13] to estimate ancestry proportions for each accession (Fig. 1c)

CLS GMD

GDsnp00688

PE MM π per kb π per kb π per kb

Discussion

Methods