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Haplotype-resolved genome assembly and resequencing provide insights into the origin and breeding of modern rose

Nature Plants volume 10, pages 1659–1671 (2024)Cite this article

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Abstract

Modern rose (Rosa hybrida) is a recently formed interspecific hybrid and has become one of the most important and widely cultivated ornamentals. Here we report the haplotype-resolved chromosome-scale genome assembly of the tetraploid R. hybrida ‘Samantha’ (‘JACmantha’) and a genome variation map of 233 Rosa accessions involving various wild species, and old and modern cultivars. Homologous chromosomes of ‘Samantha’ exhibit frequent homoeologous exchanges. Population genomic and genomic composition analyses reveal the contributions of wild Rosa species to modern roses and highlight that R. odorata and its derived cultivars are important contributors to modern roses, much like R. chinensis ‘Old Blush’. Furthermore, selective sweeps during modern rose breeding associated with major agronomic traits, including continuous and recurrent flowering, double flower, flower senescence and disease resistance, are identified. This study provides insights into the genetic basis of modern rose origin and breeding history, and offers unprecedented genomic resources for rose improvement.

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Fig. 1: Genomic landscape of R. hybrida ‘Samantha’.
Fig. 2: Population structure of 233 accessions within the genus Rosa.
Fig. 3: Genetic compositions of the ‘Samantha’ chromosomes.
Fig. 4: Genome-wide distribution of selective sweeps in R. hybrida.

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Data availability

Raw reads generated in this study have been deposited in the NCBI BioProject database under accession numbers PRJNA1108167 and PRJNA704782. The sequences and annotations of the ‘Samantha’ genome assembly are available on figshare at https://doi.org/10.6084/m9.figshare.22774097 (ref. 96). The following databases were used: BUSCO eudicot database (https://busco-data.ezlab.org/v5/data/lineages/eudicots_odb10.2024-01-08.tar.gz), GenBank common eukaryotic contaminant database (https://ftp.ncbi.nlm.nih.gov/pub/kitts/contam_in_euks.fa.gz), GenBank nt database (https://ftp.ncbi.nlm.nih.gov/blast/db/FASTA/nt.gz), InterPro database (https://www.ebi.ac.uk/interpro/download/InterPro/), UniProt (Swiss-Prot/TrEMBL) databases (https://www.uniprot.org/downloads), Repbase database (https://www.girinst.org/downloads/), Dfam database (https://www.dfam.org/releases/Dfam_3.8/families/), Fragaria ananassa ‘Yanli’ genome (https://www.rosaceae.org/Analysis/14723107), Malus domestica ‘Fuji’ genome (https://www.rosaceae.org/Analysis/15540493), Rubus idaeus ‘Joan J’ genome (https://www.rosaceae.org/Analysis/14031373), Rosa rugosa genome (https://www.rosaceae.org/Analysis/11775539), Rosa chinensis ‘Old Blush’ genome (https://www.rosaceae.org/analysis/282), Rosa wichuraiana ‘Basye’s Thornless’ genome (https://www.rosaceae.org/Analysis/13087667) and Rosa chinensis ‘Chilong Hanzhu’ genome (https://www.ncbi.nlm.nih.gov/bioproject/932466; https://doi.org/10.6084/m9.figshare.26888665.v1).

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Acknowledgements

We thank T. Lin (China Agricultural University) and Q. Gao (BGI Tech., Beijing) for helpful discussions; H. Xin and Y. Bu (Beijing Institute of Landscape Architecture) for providing computing resources and Rosa materials; the Center of Agricultural Biotechnology of Beijing Academy of Agriculture and Forestry Sciences and Golden Intelligence Biotechnology Co., Ltd. for help with flow cytometry experiments; and Wuhan Grandomics Biosciences Co., Ltd. for providing Pore-C sequencing and analysis services. This work was supported by funds from the 111 Project of the Ministry of Education (Grant no. B17043 to J.G.), the Construction of Beijing Science and Technology Innovation and Service Capacity in Top Subjects (Grant no. CEFF-PXM2019_014207_000032 to J.G.), the National Key Research and Development Program of China (Grant no. 2018YFD1000400 to J.G.), the General Project of Shenzhen Science and Technology and Innovation Commission (Grant no. 21K270360620 to Y. Li.), the National Natural Science Foundation of China (Grant no. 32372752 to Y. Li., 31772344 and 31972444 to Z.Z., and 31522049 and 31872148 to N.M.), the National Science Fund for Distinguished Young Scholars of China (Grant no. 32325046 to N.M.), the earmarked fund for CARS (Grant no. CARS-23 to N.M.), and the Postdoctoral Fellowship Program of CPSF (Grant no. GZB20240831 to T.Y.).

Author information

Author notes

  1. These authors contributed equally: Zhao Zhang, Tuo Yang, Yang Liu, Shan Wu, Honghe Sun, Jie Wu, Yonghong Li.

Authors and Affiliations

  1. Beijing Key Laboratory of Development and Quality Control of Ornamental Crops, Department of Ornamental Horticulture, College of Horticulture, China Agricultural University, Beijing, China

    Zhao Zhang, Tuo Yang, Yang Liu, Jie Wu, Haoran Ren, Shaochuan Shi, Wenyan Wang, Qi Pan, Yunhe Jiang, Xiaoming Sun, Xiaofeng Zhou, Nan Ma & Junping Gao

  2. Boyce Thompson Institute, Ithaca, NY, USA

    Shan Wu, Honghe Sun & Zhangjun Fei

  3. Plant Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, USA

    Honghe Sun

  4. School of Food and Drug, Shenzhen Polytechnic University, Shenzhen, Guangdong, China

    Yonghong Li

  5. Bioinformatics Center, Beijing University of Agriculture, Beijing, China

    Yi Zheng

  6. College of Plant Science and Technology, Beijing University of Agriculture, Beijing, China

    Yi Zheng

  7. Kunming Yang Chinese Rose Gardening Co. Ltd., Kunming, Yunnan, China

    Yuyong Yang

  8. People’s Government of Weishanzhuang Town, Daxing, Beijing, China

    Lijuan Lian

  9. Chinese Ancient Rose Garden, Beijing, China

    Shaowen Duan

  10. Yunnan Xinhaihui Flower Industry Co. Ltd., Tonghai, Yunnan, China

    Yingxiong Zhu

  11. Shanghai Academy of Agricultural Sciences, Shanghai, China

    Youming Cai

  12. College Horticulture and Landscape Architecture, Zhongkai University of Agriculture and Engineering, Guangzhou, Guangdong, China

    Hougao Zhou

  13. National Engineering Research Center for Ornamental Horticulture, Flower Research Institute of Yunnan Academy of Agricultural Sciences, Kunming, Yunnan, China

    Hao Zhang & Kaixue Tang

  14. Beijing Botanical Garden, Beijing, China

    Jiaopeng Cui

  15. Smartgenomics Technology Institute, Tianjin, China

    Dan Gao & Liyang Chen

  16. USDA-ARS Robert W Holley Center for Agriculture and Health, Ithaca, NY, USA

    Zhangjun Fei

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  1. Zhao Zhang
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Contributions

J.G., N.M., Z.F. and Z.Z. designed and coordinated the project. Y. Liu., W.W., H.R. and S.S. performed DNA extraction. T.Y. and Y. Liu. performed the flow cytometry analysis. Y.Y., L.L., S.D., Y. Zhu., Y.C., H. Zhou., H. Zhang., J.C. and K.T. contributed Rosa materials. Z.Z., Y. Liu., Y. Li., T.Y., Q.P., X.S., Y.J. and X.Z. coordinated sample collection and sequence data generation. T.Y., D.G., L.C., S.W., S.S., H.S., J.W. and Y. Zhang integrated the genome assembly and annotation. T.Y. and H.S. performed selective sweep analysis. T.Y., H.S., J.W. and Y. Zhang conducted phylogenetic and population genomic analysis. T.Y., Y. Liu., J.W., S.W., Z.Z., Y. Li, Z.F., N.M. and J.G. wrote and revised the manuscript.

Corresponding authors

Correspondence to Zhangjun Fei, Nan Ma or Junping Gao.

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The authors declare no competing interests.

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Nature Plants thanks Fabrice Foucher, Paul Arens and Diana Lopez Arias for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Phenotype and chromosome number of R. hybrida ‘Samantha®’.

a, Flower, leaf, and stem of ‘Samantha®’. b, Chromosomes of ‘Samantha®’ shown in a representative root cell.

Extended Data Fig. 2 Chromosomal synteny analysis.

Genome synteny between R. hybrida ‘Samantha®’ and R. chinensis ‘Old Blush’8.

Extended Data Fig. 3 Pore-C and Hi-C heatmaps of the assembled R. hybrida ‘Samantha®’ genome.

The signal intensity of the Pore-C heatmap is expressed as loge (Z+1), while the signal intensity of Hi-C heatmap is expressed as log10 (Z+1). Z represents the calculated interaction intensity.

Extended Data Fig. 4 Inflorescence traits of different rose accessions.

The inflorescence traits of the wild species R. multiflora have been passed down to Hybrid Multiflora and Floribunda.

Extended Data Fig. 5 Genetic organization of the 28 chromosomes of R. hybrida ‘Samantha®’.

Different colors represent genome regions derived from different potential original species.

Extended Data Fig. 6 Pore-C heatmaps showing the inversion sites of the four homologous chromosomes of Chr7.

a, Pore-C signals between homologous chromosomes of Chr7. Blue arrows indicate the inversion signal between homologous chromosomes. b, Pore-C signals in the inversion regions between homologous chromosomes. Black cross lines indicate the inversion regions. The signal intensity of the Pore-C heatmap is expressed as loge (Z+1). Z represents the calculated interaction intensity.

Extended Data Fig. 7 Collinearity analysis of the region on chromosome 7 harboring an inversion.

Four publicly available Rosa genomes, R. chinensis ‘Old Blush’8, R. chinensis ‘Chilong Hanzhu’16, R. rugosa17 and R. wichuraiana18, were used. The potential origins of this region in the ‘Samantha®’ genome are indicated with different colors.

Extended Data Fig. 8 Selection and evolution of recurrent blooming in modern roses.

a,d, π ratio and FST values in the selective sweep region containing the KSN genes. b,e, Genes in the selective sweep region. Blue boxes represent genes located on the sense strand, while yellow boxes represent genes located on the antisense strand. c,f, Heatmap of SNP genotype profiles in the selective sweep region. Maximum likelihood phylogenetic tree constructed from these SNPs is shown on the left. The rectangular boxes on the right indicate the sections to which the samples belong. Hyb, modern cultivars, R. hybrida; Syn, section Synstylae; Syn-Rm, R. moschata; Chi-Rc, R. chinensis in section Chinenses; Chi-Ro, R. odorata in section Chinenses; Rosa, section Rosa; Can, section Caninae; Cin, section Cinnamomeae; Other, sections Pimpinellifoliae, Microphyllae, Bracteatae, Banksianae, and Laevigatae.

Extended Data Fig. 9 Selection and evolution of double flower in modern roses.

a,d, π ratio and FST values in the selective sweep region containing the AP2 genes. b,e, Genes in the selective sweep region. Blue boxes represent genes located on the sense strand, while yellow boxes represent genes located on the antisense strand. c,f, Heatmap of SNP genotype profiles in the selective sweep region. Maximum likelihood phylogenetic tree constructed from these SNPs is shown on the left. The rectangular boxes on the right indicate the sections to which the samples belong. Hyb, modern cultivars, R. hybrida; Syn, section Synstylae; Syn-Rm, R. moschata; Chi-Rc, R. chinensis in section Chinenses; Chi-Ro, R. odorata in section Chinenses; Rosa, section Rosa; Can, section Caninae; Cin, section Cinnamomeae; Other, sections Pimpinellifoliae, Microphyllae, Bracteatae, Banksianae, and Laevigatae.

Extended Data Fig. 10 Selection and evolution of ethylene sensitivity in modern roses.

a, π ratio and FST values in the selective sweep region containing CTR1 and ROS1 genes. b, Genes in the selective sweep region. Blue boxes represent genes located on the sense strand, while yellow boxes represent genes located on the antisense strand. c, Heatmap of SNP genotype profiles in selective sweep regions. Maximum likelihood phylogenetic tree is shown on the left. The rectangular boxes on the right indicate the sections to which the samples belong. Hyb, modern cultivars, R. hybrida; Syn, section Synstylae; Syn-Rm, R. moschata; Chi-Rc, R. chinensis in section Chinenses; Chi-Ro, R. odorata in section Chinenses; Rosa, section Rosa; Can, section Caninae; Cin, section Cinnamomeae; Other, sections Pimpinellifoliae, Microphyllae, Bracteatae, Banksianae, and Laevigatae.

Supplementary information

Supplementary Information

Supplementary Notes 1–4 and Figs. 1–9.

Reporting Summary

Supplementary Tables

Supplementary Tables 1–15.

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Zhang, Z., Yang, T., Liu, Y. et al. Haplotype-resolved genome assembly and resequencing provide insights into the origin and breeding of modern rose. Nat. Plants 10, 1659–1671 (2024). https://doi.org/10.1038/s41477-024-01820-x

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