The genus Rosa comprises more than 100 woody species characterized by intensive hybridization, introgression, and an overall complex evolutionary history. Besides many diploid species (2n = 2x = 14) polyploids ranging from 3x to 10x are frequently found. Here we analyzed 5S ribosomal DNA in 19 species covering two subgenera and the major sections within subg. Rosa. In addition to diploids and polyploids with regular meiosis, we focused on 5x dogroses (Rosa sect. Caninae), which exhibit an asymmetric meiosis differentiating between bivalent- and univalent-forming chromosomes. Using genomic resources, we reconstructed 5S rDNA units to reveal their phylogenetic relationships. Additionally, we designed locus-specific probes derived from intergenic spacers (IGSs) and determined the position and number of 5S rDNA families on chromosomes. Two major 5S rDNA families (termed 5S_A and 5S_B, respectively) were found at variable ratios in both diploid and polyploid species including members of the early diverging subgenera, Rosa persica and Rosa minutifolia. Within subg. Rosa species of sect. Rosa amplified the 5S_A variant only, while taxa of other sections contained both variants at variable ratios. The 5S_B family was often co-localized with 35S rDNA at the nucleolar organizer regions (NOR) chromosomes, whereas the co-localization of the 5S_A family with NOR was only exceptionally observed. The allo-pentaploid dogroses showed a distinct distribution of 5S rDNA families between bivalent- and univalent-forming chromosomes. In conclusion, two divergent 5S rDNA families dominate rose genomes. Both gene families apparently arose in the early history of the genus, already 30 myrs ago, and apparently survived numerous speciation events thereafter. These observations are consistent with a relatively slow genome turnover in the Rosa genus.

Chair of Biodiversity of Higher Plants International Institute Zittau Technische Universität Dresden Zittau Germany

Department of Botany Senckenberg Museum of Natural History Görlitz Görlitz Germany

Department of Experimental Biology Faculty of Science Masaryk University Brno Czechia

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

Department of Molecular Genetics and Biotechnology Yuriy Fedkovych Chernivtsi National University Chernivtsi Ukraine

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Amosova A. V., Zoshchuk S. A., Rodionov A. V., Ghukasyan L., Samatadze T. E., Punina E. O., et al. (2019). Molecular cytogenetics of valuable Arctic and sub-Arctic pasture grass species from the PubMed DOI PMC

Benson C. W., Mao Q., Huff D. R. (2020). Global DNA methylation predicts epigenetic reprogramming and transgenerational plasticity in DOI

Blackburn K. B., Harrison J. W. H. (1921). The status of the British rose forms as determined by their cytological behaviour. DOI

Bruneau A., Starr J. R., Joly S. (2007). Phylogenetic relationships in the genus DOI

Christ H. (1873).

Crépin F. (1889). Sketch of a new classification of roses.

Cronn R. C., Zhao X., Paterson A. H., Wendel J. F. (1996). Polymorphism and concerted evolution in a tandemly repeated gene family: 5S ribosomal DNA in diploid and allopolyploid cottons. PubMed DOI

Debray K., Marie-Magdelaine J., Ruttink T., Clotault J., Foucher F., Malecot V. (2019). Identification and assessment of variable single-copy orthologous (SCO) nuclear loci for low-level phylogenomics: a case study in the genus PubMed DOI PMC

Dover G. (1982). Molecular drive: a cohesive mode of species evolution. PubMed DOI

Edelman D. W. (1975).

Eickbush T. H., Eickbush D. G. (2007). Finely orchestrated movements: evolution of the ribosomal RNA genes. PubMed DOI PMC

Fernandez-Romero M. D., Torres A. M., Millan T., Cubero J. I., Cabrera A. (2001). Physical mapping of ribosomal DNA on several species of the subgenus DOI

Fougere-Danezan M., Joly S., Bruneau A., Gao X. F., Zhang L. B. (2015). Phylogeny and biogeography of wild roses with specific attention to polyploids. PubMed DOI PMC

Fulnecek J., Lim K. Y., Leitch A. R., Kovařik A., Matyasek R. (2002). Evolution and structure of 5S rDNA loci in allotetraploid PubMed DOI

Garcia S., Borowska-Zuchowska N., Wendel J. F., Ainouche M., Kuderova A., Kovařik A. (2020). The utility of graph clustering of 5S ribosomal DNA homoeologs in plant allopolyploids, homoploid hybrids and cryptic introgressants. PubMed DOI PMC

Garcia S., Kovařik A., Leitch A. R., Garnatje T. (2016). Cytogenetic features of rRNA genes across land plants: analysis of the Plant rDNA database. PubMed DOI

Gouy M., Guindon S., Gascuel O. (2010). SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. PubMed DOI

Hemleben V., Ganal M., Gersnter J., Schiebel K., Torres R. A. (1988). “Organization and length heterogeneity of plant ribosomal RNA genes,” in

Herklotz V., Ritz C. M. (2017). Multiple and asymmetrical origin of polyploid dog rose hybrids ( PubMed DOI PMC

Herklotz V., Kovařik A., Lunerova J., Lippitsch S., Groth M., Ritz C. M. (2018). The fate of ribosomal RNA genes in spontaneous polyploid dogrose hybrids [ PubMed DOI

Joly S., Bruneau A. (2006). Incorporating allelic variation for reconstructing the evolutionary history of organisms from multiple genes: An example from PubMed DOI

Katoh K., Standley D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. PubMed DOI PMC

Kirov I. V., Van Laere K., Van Roy N., Khrustaleva L. I. (2016). Towards a FISH-based karyotype of PubMed DOI PMC

Koopman W. J. M., Wissemann V., De Cock K., Van Huylenbroeck J., De Riek J., Sabatlno G. J. H., et al. (2008). AFLP markers as a tool to reconstruct complex relationships: A case study in PubMed DOI

Kovařik A., Werlemark G., Leitch A. R., Souckova-Skalicka K., Lim Y. K., Khaitova L., et al. (2008). The asymmetric meiosis in pentaploid dogroses ( PubMed DOI

Kumar S., Stecher G., Li M., Knyaz C., Tamura K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. PubMed DOI PMC

Langmead B., Salzberg S. L. (2012). Fast gapped-read alignment with Bowtie 2. PubMed DOI PMC

Lim K. Y., Werlemark G., Matyasek R., Bringloe J. B., Sieber V., El Mokadem H., et al. (2005). Evolutionary implications of permanent odd polyploidy in the stable sexual, pentaploid of PubMed DOI

Liu C. Y., Wang G. L., Wang H., Xia T., Zhang S. Z., Wang Q. G., et al. (2015). Phylogenetic relationships in the genus DOI

Long E. O., Dawid I. B. (1980). Repeated genes in eukaryotes. PubMed DOI

Lunerova J., Herklotz V., Laudien M., Vozarova R., Groth M., Kovařik A., et al. (2020). Asymmetrical canina meiosis is accompanied by the expansion of a pericentromeric satellite in non-recombining univalent chromosomes in the genus PubMed DOI PMC

Ma Y., Crane C. F., Byrne D. H. (1997). Karyotypic relationships among some DOI

Matsumoto S., Kouchi M., Yabuki J., Kusunoki M., Ueda Y., Fukui H. (1998). Phylogenetic analyses of the genus DOI

Millan T., Osuna F., Cobos S., Torres A. M., Cubero J. I. (1996). Using RAPDs to study phylogenetic relationships in PubMed DOI

Nagylaki T. (1990). Gene conversion, linkage, and the evolution of repeated genes dispersed among multiple chromosomes. PubMed PMC

Nakamura N., Hirakawa H., Sato S., Otagaki S., Matsumoto S., Tabata S., et al. (2018). Genome structure of PubMed DOI PMC

Nieto Feliner G., Rossello J. A. (2012). “Concerted evolution of multigene families and homeologous recombination,” in

Novak P., Neumann P., Macas J. (2010). Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. PubMed DOI PMC

Novak P., Neumann P., Pech J., Steinhaisl J., Macas J. (2013). RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. PubMed DOI

Nybom H., Esselink G. D., Werlemark G., Vosman B. (2004). Microsatellite DNA marker inheritance indicates preferential pairing between two highly homologous genomes in polyploid and hemisexual dog-roses, PubMed DOI

Nybom H., Esselink G. D., Werlemark G., Leus L., Vosman B. (2006). Unique genomic configuration revealed by microsatellite DNA in polyploid dogroses, PubMed DOI

Ohta T. (1984). Some models of gene conversion for treating the evolution of multigene families. PubMed PMC

Pachl Š. (2011).

Pastova L., Belyayev A., Mahelka V. (2019). Molecular cytogenetic characterisation of PubMed DOI PMC

Pedrosa-Harand A., de Almeida C. C. S., Mosiolek M., Blair M., Schweizer D., Guerra M. (2006). Extensive ribosomal DNA amplification during Andean common bean ( PubMed DOI

Peters H., Peters H. (2013).

Raymond O., Gouzy J., Just J., Badouin H., Verdenaud M., Lemainque A., et al. (2018). The Rosa genome provides new insights into the domestication of modern roses. PubMed DOI PMC

Ritz C. M., Schmuths H., Wissemann V. (2005). Evolution by reticulation: European dogroses originated by multiple hybridization across the genus PubMed DOI

Roa F., Guerra M. (2012). Distribution of 45S rDNA sites in chromosomes of plants: structural and evolutionary implications. PubMed DOI PMC

Roberts A. V., Gladis T., Brumme H. (2009). DNA amounts of roses ( PubMed DOI

Rogers S. O., Bendich A. J. (1985). Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant-tissues. PubMed DOI

Saint-Oyant L. H., Ruttink T., Hamama L., Kirov I., Lakhwani D., Zhou N. N., et al. (2018). A high-quality genome sequence of PubMed DOI PMC

Schwarzacher T., Heslop-Harrison P. (2000).

Simon L., Rabanal F. A., Dubos T., Oliver C., Lauber D., Poulet A., et al. (2018). Genetic and epigenetic variation in 5S ribosomal RNA genes reveals genome dynamics in PubMed DOI PMC

Täckholm G. (1920). On the cytology of the genus

Tamura K. (1992). Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. PubMed

Tamura K., Tao Q., Kumar S. (2018). Theoretical foundation of the RelTime method for estimating divergence times from variable evolutionary rates. PubMed DOI PMC

Tynkevich Y. O., Volkov R. A. (2014a). Novel structural class of 5S rDNA of DOI

Tynkevich Y. O., Volkov R. A. (2014b). Structural organization of 5Sribosomal DNA in PubMed DOI

Volkov R. A., Panchuk I. I., Borisjuk N. V., Hosiawa-Baranska M., Maluszynska J., Hemleben V. (2017). Evolutional dynamics of 45S and 5S ribosomal DNA in ancient allohexaploid PubMed DOI PMC

Volkov R. A., Zanke C., Panchuk I. I., Hemleben V. (2001). Molecular evolution of 5S rDNA of DOI

Wang G. L. (2007). A study on the history of Chinese roses from ancient works and images. DOI

Weiss-Schneeweiss H., Tremetsberger K., Schneeweiss G. M., Parker J. S., Stuessy T. F. (2008). Karyotype diversification and evolution in diploid and polyploid South American PubMed DOI PMC

Wissemann V. (1999). Genetic constitution of

Wissemann V. (2003). “Conventional taxonomy (wild roses),” in

Wissemann V., Ritz C. M. (2005). The genus DOI

Xiang Y. Z., Huang C. H., Hu Y., Wen J., Li S. H., Yi T. S., et al. (2017). Evolution of Rosaceae fruit types based on nuclear phylogeny in the context of geological times and genome duplication. PubMed DOI PMC

Yokoya K., Roberts A. V., Mottley J., Lewis R., Brandham P. E. (2000). Nuclear DNA amounts in roses. DOI

Zetter R., Hofmann C., Draxler I., Durango, de Cabrera J., Vergel M., et al. (1999). A rich Middle Eocene Microflora at Arroyo de los Mineros, near Cañadón Beta, NE Tierra del Fuego Province, Argentina.

Zhang J., Esselink G. D., Che D., Fougere-Danezan M., Arens P., Smulders M. J. M. (2013). The diploid origins of allopolyploid rose species studied using single nucleotide polymorphism haplotypes flanking a microsatellite repeat. DOI

Zhu Z. M., Gao X. F., Fougere-Danezan M. (2015). Phylogeny of PubMed DOI

Bimodal centromeres in pentaploid dogroses shed light on their unique meiosis

First insight into the genomes of the Pulmonaria officinalis group (Boraginaceae) provided by repeatome analysis and comparative karyotyping

Epigenetic histone H3 phosphorylation marks discriminate between univalent- and bivalent-forming chromosomes during canina asymmetrical meiosis

Analysis of 5S rDNA Genomic Organization Through the RepeatExplorer2 Pipeline: A Simplified Protocol

Power and Weakness of Repetition - Evaluating the Phylogenetic Signal From Repeatomes in the Family Rosaceae With Two Case Studies From Genera Prone to Polyploidy and Hybridization (Rosa and Fragaria)

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