Comparative population genomics reveals convergent and divergent selection in the apricot-peach-plum-mei complex

Abstract

The economically significant genus Prunus includes fruit and nut crops that have been domesticated for shared and specific agronomic traits; however, the genomic signals of convergent and divergent selection have not been elucidated. In this study, we aimed to detect genomic signatures of convergent and divergent selection by conducting comparative population genomic analyses of the apricot-peach-plum-mei (APPM) complex, utilizing a haplotype-resolved telomere-to-telomere (T2T) genome assembly and population resequencing data. The haplotype-resolved T2T reference genome for the plum cultivar was assembled through HiFi and Hi-C reads, resulting in two haplotypes 251.25 and 251.29 Mb in size, respectively. Comparative genomics reveals a chromosomal translocation of ∼ 1.17 Mb in the apricot genomes compared with peach, plum, and mei. Notably, the translocation involves the D locus, significantly impacting titratable acidity (TA), pH, and sugar content. Population genetic analysis detected substantial gene flow between plum and apricot, with introgression regions enriched in post-embryonic development and pollen germination processes. Comparative population genetic analyses revealed convergent selection for stress tolerance, flower development, and fruit ripening, along with divergent selection shaping specific crop, such as somatic embryogenesis in plum, pollen germination in mei, and hormone regulation in peach. Notably, selective sweeps on chromosome 7 coincide with a chromosomal collinearity from the comparative genomics, impacting key fruit-softening genes such as PG, regulated by ERF and RMA1H1. Overall, this study provides insights into the genetic diversity, evolutionary history, and domestication of the APPM complex, offering valuable implications for genetic studies and breeding programs of Prunus crops.

Acknowledgements

We are grateful to the Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences for providing the high-performance computing platforms during this study. This work was financially supported by the Guizhou Provincial Science and Technology Projects of China ([2022]Zhongdian018, YQK[2023]008), the National Guidance Foundation for Local Science and Technology Development of China (Grant No. 2023-009), and the Science Fund Program for Distinguished Young Scholars of the National Natural Science Foundation of China (Overseas) to Yongfeng Zhou. We also thank all members of the Zhou Lab for their valuable discussions and constructive comments.

Author contributions

G.Q., K.C., and Y.Z. were responsible for conceiving and designing the research. X.Y., Y.S., and S.H. contributed to writing the manuscript. X.Y. and S.H. were responsible for collecting and updating the genome assemblies, while Y.S. performed the gene annotation. All authors contributed to the data collection and/or bioinformatics analyses. Y.M. and Q.H. provided the experimental materials. All authors have reviewed and approved the final manuscript.

Data availability

The PS_T2T raw genome sequencing reads were available from the NCBI under project ID PRJNA1000098. All raw sequence data and assembly have been deposited in the National Genomics Data Center (NGDC) Genome Sequence Archive (GSA) (https://ngdc.cncb.ac.cn/gsa/), with BioProject number PRJCA018700. The assembly and annotation have been deposited in zenodo: https://zenodo.org/records/10570999.

Conflict of interest

The authors declare that they have no competing interests.

Supplementary data

Supplementary data are available at Horticulture Research online.

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