Frequent germplasm exchanges drive the high genetic diversity of Chinese-cultivated common apricot germplasm

Zhang et al. Horticulture Research (2021)8:215 https://doi.org/10.1038/s41438-021-00650-8 ARTICLE Horticulture Research www.nature.com/hortres Open Access Frequent germplasm exchanges drive the high genetic diversity of Chinese-cultivated common apricot germplasm 1234567890():,; 1234567890():,; 1234567890():,; 1234567890():,; Qiuping Zhang 1, Diyang Zhang 2, Kang Yu 3, Jingjing Ji3, Ning Liu1, Yuping Zhang1, Ming Xu1, Yu-Jun Zhang1, Xiaoxue Ma1, Shuo Liu1, Wei-Hong Sun2, Xia Yu2, Wenqi Hu2, Si-Ren Lan2, Zhong-Jian Liu2,4,5 ✉ and Weisheng Liu1 ✉ Abstract The genetic diversity of germplasm is critical for exploring genetic and phenotypic resources and has important implications for crop-breeding sustainability and improvement. However, little is known about the factors that shape and maintain genetic diversity. Here, we assembled a high-quality chromosome-level reference of the Chinese common apricot ‘Yinxiangbai’, and we resequenced 180 apricot accessions that cover four major ecogeographical groups in China and other accessions from occidental countries. We concluded that Chinese-cultivated common apricot germplasms possessed much higher genetic diversity than those cultivated in Western countries. We also detected seven migration events among different apricot groups, where 27% of the genome was identified as being introgressed. Remarkably, we demonstrated that these introgressed regions drove the current high level of germplasm diversity in Chinese-cultivated common apricots by introducing different genes related to distinct phenotypes from different cultivated groups. Our results highlight the consideration that introgressed regions may provide an important reservoir of genetic resources that can be used to sustain modern breeding programs. Introduction Crop germplasms, particularly those from the centers of origin, provide critical resources for exploring and conserving genetic and phenotypic diversity for breeding applications1,2. The diversity of crop germplasm has been suggested to have important implications for breeding sustainability and crop improvement, as it determines the sustained ability of plant breeders to develop new highquality varieties3. Hence, it is essential to characterize the factors driving and maintaining germplasm diversity in Correspondence: Zhong-Jian Liu () or Weisheng Liu () 1 Liaoning Institute of Pomology, Yingkou 115009, China 2 Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization at College of Landscape Architecture, Fujian Agriculture and Forestry University, Fuzhou 350002, China Full list of author information is available at the end of the article These authors contributed equally: Qiuping Zhang, Diyang Zhang, Kang Yu, and Jingjing Ji crops, a consideration that has largely been ignored in previous plant-breeding research. The common apricot (Prunus armeniaca L.) belongs to the subgenus Prunophora of the genus Prunus in the Rosaceae family and has been widely grown in temperate zones, primarily in its cultivated form. Documented evidence suggests that common apricots originate from China and Central Asia and are dispersed outward4–6. The common apricot germplasm in China has been speculated to be the oldest, most diversified, and the most currently underexplored resource7. Recorded in ancient Chinese literature, the first apricot-cultivation event occurred approximately 3000–4000 years ago8, and this represents the earliest apricot domestication in the world. The genetic structure of Chinese apricots that was revealed by molecular markers supported the existence of five major ecological groups, including those from North China (NC), Northwest China (NWC), Northeast China (NEC), Southeast China (SEC), and Xinjiang (XJ), with © The Author(s) 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Zhang et al. Horticulture Research (2021)8:215 frequent germplasm exchanges occurring among these groups9. A long history of cultivation in combination with varied ecological groups and frequent germplasm-migrant events enables Chinese apricot to serve as an attractive model to investigate the factors responsible for germplasm diversity in crops. Here, we report a chromosomal-level genome assembly of P. armeniaca “Yinxiangbai”, and we resequenced the whole genomes of 150 apricot accessions from China that covered four of the five major ecological groups and 30 occidental accessions. In this study, we addressed the population genomics of apricots with an emphasis on germplasm-exchange events, and we further elucidated the role of this process in shaping the germplasm diversity of the common apricot in China. Results Genome assembly and annotation Prunus armeniaca (“Yinxiangbai”), a native diploid cultivar from Lintong, Shanxi Province, North China, was selected for whole-genome sequencing. We generated a total of 45.73 Gb of raw data with a 350-bp insert-size library and 47.52 Gb (PacBio) and 82.37 Gb (Nanopore) of long reads (Supplementary Table 1). A 17-mer analysis revealed that P. armeniaca “Yinxiangbai” possessed a genome size of 264.4 Mb with a heterozygosity rate of 0.99% (Supplementary Fig. 1). The integration of the short and long reads yielded a final genome size of 251.19 Mb and a contig N50 of 4.04 Mb (Supplementary Table 2), both parameters were much larger than those from previously published reports (221.9 Mb with a contig N50 = 1.02 Mb)10. The assembled contigs were further anchored to eight linkage groups using linkage maps (Supplementary Fig. 2). Further application of the Hi-C data yielded a total length of 251.19 Mb (Supplementary Table 3), a scaffold N50 of 30.98 Mb, and a contig-anchoring rate of 97.04%, thus representing the highest-quality reference genome ever reported for the Prunus genus (Supplementary Fig. 3; Supplementary Table 3). The BUSCO (Benchmarking Universal Single-Copy Orthologs) assessment11 revealed that the assembled genome could represent up to 96.20% of the complete P. armeniaca “Yinxiangbai” genome (Supplementary Table 4). Gene model prediction identified 29,230 protein-coding genes (Supplementary Table 5), and this was comparable to that of other Prun (...truncated)