Sexual reproduction relies on meiotic chromosome pairing to form bivalents, a process that is complicated in polyploids owing to the presence of multiple subgenomes1. Uneven ploidy mostly results in sterility due to unbalanced chromosome pairing and segregation during meiosis. However, pentaploid dogroses (Rosa sect. Caninae; 2n = 5x = 35) achieve stable sexual reproduction through a unique mechanism: 14 chromosomes form bivalents and are transmitted biparentally, while the remaining 21 chromosomes are maternally inherited as univalents2,3. Despite being studied for over a century, the role of centromeres in this process has remained unclear. Here we analyse haplotype-resolved chromosome-level genome assemblies for three pentaploid dogroses. Subgenome phasing revealed a bivalent-forming subgenome with two highly homozygous chromosome sets and three divergent subgenomes lacking homologous partners, therefore explaining their meiotic behaviour. Comparative analyses of chromosome synteny, phylogenetic relationships and centromere composition indicate that the subgenomes originated from two divergent clades of the genus Rosa. Pollen genome analysis shows that subgenomes from different evolutionary origins form bivalents, supporting multiple origins of dogroses and highlighting variation in subgenome contributions. We reveal that bivalent-forming centromeres are enriched with ATHILA retrotransposons, contrasting with larger tandem-repeat-based centromeres mainly found in univalents. This centromere structural bimodality possibly contributes to univalent drive during female meiosis. Our findings provide insights into the unique reproductive strategies of dogroses, advancing our understanding of genome evolution, centromere diversity and meiotic mechanisms in organisms with asymmetrical inheritance systems.

Cluster of Excellence on Plant Sciences Heinrich Heine University Düsseldorf Germany

Department of Chromosome Biology Max Planck Institute for Plant Breeding Research Cologne Germany

Department of Molecular Epigenetics Institute of Biophysics Czech Academy of Sciences Brno Czech Republic

German Centre for Integrative Biodiversity Research Halle Jena Leipzig Leipzig Germany

Institute of Botany Systematic Botany Group Justus Liebig University Gießen Germany

International Institute Zittau TUD Dresden University of Technology Zittau Germany

Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben Seeland Germany

Max Planck Genome Centre Cologne Max Planck Institute for Plant Breeding Research Cologne Germany

Senckenberg Museum for Natural History Görlitz Senckenberg Leibniz Institution for Biodiversity and Earth System Research Görlitz Germany

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Bomblies, K. Learning to tango with four (or more): the molecular basis of adaptation to polyploid meiosis. PubMed PMC

Blackburn, K. B. & Harrison, J. H. W. The status of the British rose forms as determined by their cytological behaviour. DOI

Täckholm, G. Zytologische studien über die gattung

Van de Peer, Y., Maere, S. & Meyer, A. The evolutionary significance of ancient genome duplications. PubMed DOI

Mercier, R., Mezard, C., Jenczewski, E., Macaisne, N. & Grelon, M. The molecular biology of meiosis in plants. PubMed DOI

Wang, Y. X. & Copenhaver, G. P. in PubMed

Pelé, A., Rousseau-Gueutin, M. & Chevre, A. M. Speciation success of polyploid plants closely relates to the regulation of meiotic recombination. PubMed PMC

Herben, T., Suda, J. & Klimešová, J. Polyploid species rely on vegetative reproduction more than diploids: a re-examination of the old hypothesis. PubMed DOI PMC

Wang, Y. Z. & Underwood, C. J. Apomixis. PubMed

Deb, S. K., Edger, P. P., Pires, J. C. & McKain, M. R. Patterns, mechanisms, and consequences of homoeologous exchange in allopolyploid angiosperms: a genomic and epigenomic perspective. PubMed DOI

Moore, G. Meiosis in allopolyploids—the importance of ‘Teflon’ chromosomes. PubMed DOI

Debray, K. et al. Unveiling the patterns of reticulated evolutionary processes with phylogenomics: hybridization and polyploidy in the genus PubMed DOI

Fougere-Danezan, M., Joly, S., Bruneau, A., Gao, X. F. & Zhang, L. B. Phylogeny and biogeography of wild roses with specific attention to polyploids. PubMed DOI PMC

Raymond, O. et al. The PubMed DOI PMC

Saint-Oyant, L. H. et al. A high-quality genome sequence of PubMed DOI PMC

Zhang, X. et al. Haplotype-resolved genome assembly of the diploid PubMed DOI PMC

Chen, F. et al. A chromosome-level genome assembly of rugged rose ( PubMed PMC

Bourke, P. M. et al. Partial preferential chromosome pairing is genotype dependent in tetraploid rose. PubMed DOI

Zhang, Z. et al. Haplotype-resolved genome assembly and resequencing provide insights into the origin and breeding of modern rose. PubMed DOI

Lunerová, L. et al. Asymmetrical canina meiosis is accompanied by the expansion of a pericentromeric satellite in non-recombining univalent chromosomes. PubMed DOI PMC

Lim, K. Y. et al. Evolutionary implications of permanent odd polyploidy in the stable sexual, pentaploid of PubMed DOI

Blackburn, K. B. Chromosomes and classification in the genus DOI

Täckholm, G. On the cytology of the genus

Nybom, H., Esselink, G. D., Werlemark, G., Leus, L. & Vosman, B. Unique genomic configuration revealed by microsatellite DNA in polyploid dogroses, PubMed DOI

Nybom, H., Esselink, G. D., Werlemark, G. & Vosman, B. Microsatellite DNA marker inheritance indicates preferential pairing between two highly homologous genomes in polyploid and hemisexual dog-roses, PubMed DOI

Ritz, C. M. & Wissemann, V. Microsatellite analyses of artificial and spontaneous dogrose hybrids reveal the hybridogenic origin of PubMed DOI

Ritz, C. M., Köhnen, I., Groth, M., Theißen, G. & Wissemann, V. To be or not to be the odd one out—allele-specific transcription in pentaploid dogroses ( PubMed DOI PMC

Ritz, C. M., Schmuths, H. & Wissemann, V. Evolution by reticulation: European dogroses originated by multiple hybridization across the genus PubMed DOI

Wissemann, V. Molecular evidence for allopolyploid origin in the

Ballmer, D.

Bruneau, A., Starr, J. R. & Joly, S. Phylogenetic relationships in the genus DOI

Debray, K. et al. Unveiling the patterns of reticulated evolutionary processes with phylogenomics: hybridization and polyploidy in the genus PubMed

Wissemann, V. & Ritz, C. M. The genus DOI

Herklotz, V. et al. The fate of ribosomal RNA genes in spontaneous polyploid dogrose hybrids ( PubMed DOI

Vozárová, R. et al. Ancient origin of two 5S rDNA families dominating in the genus PubMed DOI PMC

Henikoff, S., Ahmad, K. & Malik, H. S. The centromere paradox: stable inheritance with rapidly evolving DNA. PubMed DOI

Henikoff, S. & Malik, H. S. Centromeres: selfish drivers. PubMed DOI

Kolarčik, V., Zozomová-Lihová, J., Ducár, E. & Martonfi, P. Evolutionary significance of hybridization in DOI

Dedukh, D. et al. A cyclical switch of gametogenic pathways in hybrids depends on the ploidy level. PubMed PMC

Dedukh, D. et al. Maintenance of pure hybridogenetic water frog populations: genotypic variability in progeny of diploid and triploid parents. PubMed PMC

Jia, K. H. et al. SubPhaser: a robust allopolyploid subgenome phasing method based on subgenome-specific PubMed DOI

Kolarčik, V., Kocova, V. & Vaskova, D. Flow cytometric seed screen data are consistent with models of chromosome inheritance in asymmetrically compensating allopolyploids. PubMed DOI

Wissemann, V. & Hellwig, F. H. Reproduction and hybridisation in the genus DOI

Reichel, K. et al. Untangling the hedge: genetic diversity in clonally and sexually transmitted genomes of European wild roses, PubMed DOI PMC

Herklotz, V. & Ritz, C. M. Multiple and asymmetrical origin of polyploid dog rose hybrids ( PubMed PMC

Naish, M. et al. The genetic and epigenetic landscape of the PubMed DOI PMC

Wlodzimierz, P. et al. Cycles of satellite and transposon evolution in PubMed

Oliveira, L. et al. KNL1 and NDC80 represent new universal markers for the detection of functional centromeres in plants. PubMed

Blackhurst, H. T. Cytogenetic studies on

Malik, H. S. & Henikoff, S. Major evolutionary transitions in centromere complexity. PubMed DOI

Fishman, L. & Saunders, A. Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers. PubMed DOI

d’Erfurth, I. et al. Turning meiosis into mitosis. PubMed DOI PMC

Lukaszewski, A. J. Behavior of centromeres in univalents and centric misdivision in wheat. PubMed DOI

Wulff, H. D. Über das spontane Auftreten einer Canina-Meiosis bei der Mikrosporogenese der diploiden DOI

Cheng, H. Y., Concepcion, G. T., Feng, X. W., Zhang, H. W. & Li, H. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. PubMed DOI PMC

Ghurye, J. et al. Integrating Hi-C links with assembly graphs for chromosome-scale assembly. PubMed PMC

Manni, M., Berkeley, M. R., Seppey, M., Simao, F. A. & Zdobnov, E. M. BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. PubMed DOI PMC

Rhie, A., Walenz, B. P., Koren, S. & Phillippy, A. M. Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies. PubMed DOI PMC

Herklotz, V. & Ritz, C. M. Spontane Hybridisierung von Hundsrosen (

Marcais, G. & Kingsford, C. A fast, lock-free approach for efficient parallel counting of occurrences of PubMed DOI PMC

Ranallo-Benavidez, T. R., Jaron, K. S. & Schatz, M. C. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. PubMed PMC

Jin, J. J. et al. GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. PubMed PMC

Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. PubMed DOI PMC

Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. PubMed DOI PMC

Camacho, C. et al. BLAST+: architecture and applications. PubMed DOI PMC

Tillich, M. et al. GeSeq—versatile and accurate annotation of organelle genomes. PubMed DOI PMC

Chan, P. P., Lin, B. Y., Mak, A. J. & Lowe, T. M. tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes. PubMed DOI PMC

Small, I. & Castleden, I. Chloë v0.1.0 (GitHub); https://github.com/ian-small/chloe (2020).

Shen, W., Le, S., Li, Y. & Hu, F. SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PubMed DOI PMC

Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. PubMed DOI PMC

Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. PubMed DOI PMC

Soderlund, C., Bomhoff, M. & Nelson, W. SyMAP v3.4: a turnkey synteny system with application to plant genomes. PubMed DOI PMC

Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. PubMed DOI PMC

Wickham, H.

Goel, M., Sun, H. Q., Jiao, W. B. & Schneeberger, K. SyRI: finding genomic rearrangements and local sequence differences from whole-genome assemblies. PubMed PMC

Li, H. Minimap2: pairwise alignment for nucleotide sequences. PubMed DOI PMC

Li, H. New strategies to improve minimap2 alignment accuracy. PubMed DOI PMC

Zhang, J. X. et al. The high-quality genome of diploid strawberry ( PubMed DOI PMC

Lovell, J. T. et al. GENESPACE tracks regions of interest and gene copy number variation across multiple genomes. PubMed DOI PMC

Wang, Y. P. et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. PubMed PMC

Emms, D. M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. PubMed PMC

Lyons, E. & Freeling, M. How to usefully compare homologous plant genes and chromosomes as DNA sequences. PubMed DOI

Lyons, E. et al. Finding and comparing syntenic regions among PubMed DOI PMC

Kielbasa, S. M., Wan, R., Sato, K., Horton, P. & Frith, M. C. Adaptive seeds tame genomic sequence comparison. PubMed DOI PMC

Joyce, B. L. et al. FractBias: a graphical tool for assessing fractionation bias following polyploidy. PubMed DOI

Pertea, G. & Pertea, M. GFF utilities: GffRead and GffCompare. PubMed DOI PMC

Rice, P., Longden, I. & Bleasby, A. EMBOSS: the European Molecular Biology Open Software Suite. PubMed DOI

Shulaev, V. et al. The genome of woodland strawberry ( PubMed DOI PMC

Suyama, M., Torrents, D. & Bork, P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. PubMed DOI PMC

Yang, Z. H. PAML: a program package for phylogenetic analysis by maximum likelihood. PubMed

Yang, Z. H. & Nielsen, R. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. PubMed DOI

R Core Team.

Matthews, J. V., Westgate, J. A., Ovenden, L., Carter, L. D. & Fouch, T. Stratigraphy, fossils, and age of sediments at the upper pit of the Lost Chicken gold mine: new information on the late Pliocene environment of east central Alaska. DOI

Matthews, J. V. & Ovenden, L. E. Late Tertiary plant macrofossils from localities in Arctic/Subarctic North America: a review of the data. DOI

Darling, A. E., Mau, B. & Perna, N. T. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PubMed PMC

Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. PubMed DOI PMC

Ellinghaus, D., Kurtz, S. & Willhoeft, U. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. PubMed DOI PMC

Xu, Z. & Wang, H. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. PubMed DOI PMC

Zhang, R. G. et al. TEsorter: an accurate and fast method to classify LTR-retrotransposons in plant genomes. PubMed PMC

Vitte, C., Panaud, O. & Quesneville, H. LTR retrotransposons in rice ( PubMed DOI PMC

Cuizhi, G. & Robertson, K. in

Henker, H. in

Lewis, W., Ertter, B. & Bruneau, A. in

Kron, P. & Husband, B. C. Using flow cytometry to estimate pollen DNA content: improved methodology and applications. PubMed DOI PMC

Galbraith, D. W. et al. Rapid flow cytometric analysis of the cell cycle in intact plant tissues. PubMed DOI

Doyle, J. J. & Doyle, J. L. A rapid DNA isolation procedure for small quantities of fresh leaf tissue.

Debray, K. et al. Identification and assessment of variable single-copy orthologous (SCO) nuclear loci for low-level phylogenomics: a case study in the genus PubMed PMC

Deorowicz, S., Kokot, M., Grabowski, S. & Debudaj-Grabysz, A. KMC 2: fast and resource-frugal PubMed DOI

Kokot, M., Dlugosz, M. & Deorowicz, S. KMC 3: counting and manipulating PubMed DOI

Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. PubMed DOI PMC

Kamneva, O. K. et al. Evaluating allopolyploid origins in strawberries ( PubMed PMC

Danecek, P. et al. Twelve years of SAMtools and BCFtools. PubMed PMC

Van der Auwera, G. & O’Connor, B.

Poplin, R. et al. Scaling accurate genetic variant discovery to tens of thousands of samples. Preprint at

Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. PubMed DOI PMC

Shen, W., Le, S., Li, Y. & Hu, F. Q. SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PubMed DOI PMC

Price, R. J. et al. Chromosome-scale genome sequence assemblies of the ‘Autumn Bliss’ and ‘Malling Jewel’ cultivars of the highly heterozygous red raspberry PubMed PMC

Edger, P. P. et al. Reply to: Revisiting the origin of octoploid strawberry. PubMed DOI PMC

Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. PubMed DOI PMC

Sweeten, A. P., Schatz, M. C. & Phillippy, A. M. ModDotPlot—rapid and interactive visualization of tandem repeats. PubMed PMC

Stiehler, F. et al. Helixer: cross-species gene annotation of large eukaryotic genomes using deep learning. PubMed PMC

Novák, P., Neumann, P. & Macas, J. Global analysis of repetitive DNA from unassembled sequence reads using RepeatExplorer2. PubMed DOI

Novák, P., Hoštáková, N., Neumann, P. & Macas, J. DANTE and DANTE_LTR: lineage-centric annotation pipelines for long terminal repeat retrotransposons in plant genomes. PubMed PMC

RepeatMasker Open v.4.0 (2013–2015).

Kim, D., Paggi, J. M., Park, C., Bennett, C. & Salzberg, S. L. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. PubMed DOI PMC

Bolger, M., Schwacke, R. & Usadel, B. MapMan visualization of RNA-Seq data using Mercator4 functional annotations. PubMed DOI

Putri, G. H., Anders, S., Pyl, P. T., Pimanda, J. E. & Zanini, F. Analysing high-throughput sequencing data in Python with HTSeq 2.0. PubMed DOI PMC

Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. PubMed DOI PMC

Reimer, J. J. & Turck, F. Genome-wide mapping of protein-DNA interaction by chromatin immunoprecipitation and DNA microarray hybridization (ChIP-chip). Part A: ChIP-chip molecular methods. PubMed DOI

Ramirez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. PubMed DOI PMC

Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). PubMed DOI PMC

Lopez-Delisle, L. et al. pyGenomeTracks: reproducible plots for multivariate genomic datasets. PubMed DOI PMC

Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. DOI

Pedersen, T. L. patchwork: the composer of plots. R package version 1.3.0; 10.32614/CRAN.package.patchwork (2024).

Wickham, H., Vaughan, D., Girlich, M. & Ushey, K. tidyr: tidy messy data. R package version 1.3.1; 10.32614/CRAN.package.tidyr (2024).

Wickham, H., François, R., Henry, L., Müller, K. & Vaughan, D. dplyr: a grammar of data manipulation. R package version 1.1.4 (2023).

Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. PubMed DOI PMC

Hurel, A. et al. A cytological approach to studying meiotic recombination and chromosome dynamics in PubMed DOI

Nascimento, T. & Pedrosa-Harand, A. High rates of structural rearrangements have shaped the chromosome evolution in dysploid beans. PubMed

Herklotz, V. et al. Three haplotype-resolved pentaploid Rosa assemblies with assembled and extracted single copy orthologue (SCO) sequences from