Genome of tetraploid sour cherry (Prunus cerasus L.) ‘Montmorency’ identifies three distinct ancestral Prunus genomes

Abstract

Sour cherry (Prunus cerasus L.) is a valuable fruit crop in the Rosaceae family and a hybrid between progenitors closely related to extant Prunus fruticosa (ground cherry) and Prunus avium (sweet cherry). Here we report a chromosome-scale genome assembly for sour cherry cultivar Montmorency, the predominant cultivar grown in the USA. We also generated a draft assembly of P. fruticosa to use alongside a published P. avium sequence for syntelog-based subgenome assignments for ‘Montmorency’ and provide compelling evidence P. fruticosa is also an allotetraploid. Using hierarchal k-mer clustering and phylogenomics, we show ‘Montmorency’ is trigenomic, containing two distinct subgenomes inherited from a P. fruticosa-like ancestor (A and A’) and two copies of the same subgenome inherited from a P. avium-like ancestor (BB). The genome composition of ‘Montmorency’ is AA’BB and little-to-no recombination has occurred between progenitor subgenomes (A/A’ and B). In Prunus, two known classes of genes are important to breeding strategies: the self- incompatibility loci (S-alleles), which determine compatible crosses, successful fertilization, and fruit set, and the Dormancy Associated MADS-box genes (DAMs), which strongly affect dormancy transitions and flowering time. The S-alleles and DAMs in ‘Montmorency’ and P. fruticosa were manually annotated and support subgenome assignments. Lastly, the hybridization event ‘Montmorency’ is descended from was estimated to have occurred less than 1.61 million years ago, making sour cherry a relatively recent allotetraploid. The ‘Montmorency’ genome highlights the evolutionary complexity of the genus Prunus and will inform future breeding strategies for sour cherry, comparative genomics in the Rosaceae, and questions regarding neopolyploidy.

Acknowledgements

We thank Dr. Shujun Ou for his assistance in running EDTA, and all members of the Aiden Lab and Dr. Ching Man Wai for their help in operating Juicer and 3D DNA. We are also grateful to Dr. Jose Ramon Planta and Dr. Jie Wang for their help with defusion, and to Dr. Nathan Dunn and Dr. Garrett Stevens for guidance with installing and navigating Apollo. Finally, we appreciate Chloe Grabb for her assistance with manual gene annotation and Dr. Pat Edger for his advice on all phylogenomic analyses. This research was funded by AgBioResearch Project GREEEN grant GR19-046, the United States Department of Agriculture National Institute of Food and Agriculture (USDA-NIFA) project 2014-51181-22378 and USDA-NIFA HATCH project 1013242.

Authors’ contributions

C.A.H., A.F.I., and R.V. conceptualized the experiments. C.Z.G. performed genome assembly, annotation, subgenome assignment using orthologs, and divergence time estimate analyses. K.B.R. performed the k-mer hierarchal clustering, K_s analysis, synteny, DAM gene phylogenetic analyses, and S-allele alignments. K.L.C. provided expertise and assistance with annotation and contributed code. C.Z.G., K.B.R., and A.F.I. wrote the manuscript. All authors assisted with editing the manuscript.

Data availability

The datasets supporting the conclusions of this article are available in the Genomic Database for Rosaceae (GDR) https:// www.rosaceae.org/ and NCBI’s Sequence Retrieval Archive (SRA) under BioProject number PRJNA922242 (raw sequence data). Scripts and example files associated with genome assembly, annotation, gene function predictions, subgenome assignment analyses, and r8s estimates can be found at https://github.com/ goeckeritz/Montmorency_genome. Scripts for k-mer hierarchal clustering, K_s analysis, synteny, DAM gene phylogenetic analyses, and S-allele alignments can be found at https://github.com/ KEBRhoades/Montmorency_genome.

Conflict of interests statement

None declared.

Supplementary data

Supplementary data is available at Horticulture Research online.

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