BACKGROUND AND AIMS: Despite their abundant odd-ploidy (2n = 5x = 35), dogroses (Rosa sect. Caninae) are capable of sexual reproduction due to their unique meiosis. During canina meiosis, two sets of chromosomes form bivalents and are transmitted by male and female gametes, whereas the remaining chromosomes form univalents and are exclusively transmitted by the egg cells. Thus, the evolution of chromosomes is expected to be driven by their behaviour during meiosis. METHODS: To gain insight into differential chromosome evolution, fluorescence in situ hybridization was conducted for mitotic and meiotic chromosomes in four dogroses (two subsections) using satellite and ribosomal DNA probes. By exploiting high-throughput sequencing data, we determined the abundance and diversity of the satellite repeats in the genus Rosa by analysing 20 pentaploid, tetraploid and diploid species in total. KEY RESULTS: A pericentromeric satellite repeat, CANR4, was found in all members of the genus Rosa, including the basal subgenera Hulthemia and Hesperhodos. The satellite was distributed across multiple chromosomes (5-20 sites per mitotic cell), and its genomic abundance was higher in pentaploid dogroses (2.3 %) than in non-dogrose species (1.3 %). In dogrose meiosis, univalent chromosomes were markedly enriched in CANR4 repeats based on both the number and the intensity of the signals compared to bivalent-forming chromosomes. Single-nucleotide polymorphisms and cluster analysis revealed high intragenomic homogeneity of the satellite in dogrose genomes. CONCLUSIONS: The CANR4 satellite arose early in the evolution of the genus Rosa. Its high content and extraordinary homogeneity in dogrose genomes is explained by its recent amplification in non-recombining chromosomes. We hypothesize that satellite DNA expansion may contribute to the divergence of univalent chromosomes in Rosa species with non-symmetrical meiosis.

Department of Botany Senckenberg Museum of Natural History Görlitz Görlitz Germany

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

Leibniz Institute on Ageing Fritz Lipmann Institute Jena Germany

Masaryk University Faculty of Science Brno Czech Republic

Technical University Dresden International Institute Zittau Chair of Biodiversity of Higher Plants Zittau Germany

Komentář v

Ann Bot. 2020 Jun 1;125(7):v-vi. doi: 10.1093/aob/mcaa075. PubMed

Zobrazit více v PubMed

Akasaka M, Ueda Y, Koba T. 2003. Karyotype analysis of wild rose species belonging to septets B, C, and D by molecular cytogenetic method. Breeding Science 53: 177–182.

Alix K, Gerard PR, Schwarzacher T, Heslop-Harrison JS. 2017. Polyploidy and interspecific hybridization: partners for adaptation, speciation and evolution in plants. Annals of Botany 120:183–194. PubMed PMC

Barker MS, Arrigo N, Baniaga AE, Li Z, Levin DA. 2016. On the relative abundance of autopolyploids and allopolyploids. New Phytologist 210: 391–398. PubMed

Belyayev A, Paštová L, Fehrer J, Josefiová J, Chrtek J, Mráz P. 2018. Mapping of Hieracium (Asteraceae) chromosomes with genus-specific satDNA elements dervied from next generation sequencing data. Plant Systematics and Evolution 304: 387–396.

Blackburn KB. 1925. Chromosomes and classification in the genus Rosa. American Naturalist 59: 200–204.

Blackburn KB, Harrison JHW. 1921. The status of the British rose forms as determined by their cytological behaviour. Annals of Botany 35: 159–188.

Bruneau A, Starr JR, Joly S. 2007. Phylogenetic relationships in the genus Rosa: new evidence from chloroplast DNA sequences and an appraisal of current knowledge. Systematic Botany 32: 366–378.

Ding XL, Xu TL, Wang J, et al. . 2016. Distribution of 45S rDNA in modern rose cultivars (Rosa hybrida), Rosa rugosa, and their interspecific hybrids revealed by fluorescence in situ hybridization. Cytogenetic and Genome Research 149: 226–235. PubMed

Dodsworth S, Chase MW, Kelly LJ, et al. . 2015. Genomic repeat abundances contain phylogenetic signal. Systematic Biology 64: 112–126. PubMed PMC

Dumolin S, Demesure B, Petit RJ. 1995. Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR method. Theoretical and Applied Genetics 91: 1253–1256. PubMed

Emadzade K, Jang TS, Macas J, et al. . 2014. Differential amplification of satellite PaB6 in chromosomally hypervariable Prospero autumnale complex (Hyacinthaceae). Annals of Botany 114: 1597–1608. PubMed PMC

Fernandez-Romero MD, Torres AM, Millan T, Cubero JI, Cabrera A. 2001. Physical mapping of ribosomal DNA on several species of the subgenus Rosa. Theoretical and Applied Genetics 103: 835–838.

Ferus P, Pachl Š, Ďurišová L, Bartošová-Krajčovičová D, Rovna K. 2013. Is there any relation between quantitative traits interesting for ornamental breeding and genome size in dog roses (Rosa sect. Caninae)? Folia Oecologica 40: 11–21.

Fougere-Danezan M, Joly S, Bruneau A, Gao XF, Zhang LB. 2015. Phylogeny and biogeography of wild roses with specific attention to polyploids. Annals of Botany 115: 275–291. PubMed PMC

Frank AC, Amiri H, Andersson SGE. 2002. Genome deterioration: loss of repeated sequences and accumulation of junk DNA. Genetica 115: 1–12. PubMed

Galtier N, Gouy M, Gautier C. 1996. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Computer Applications in the Biosciences 12: 543–548. PubMed

Garcia S, Garnatje T, Kovařík A. 2012. Plant rDNA database: ribosomal DNA loci information goes online. Chromosoma 121: 389–394. PubMed

Garrido-Ramos MA. 2017. Satellite DNA: an evolving topic. Genes 8: 230 PubMed PMC

Grandont L, Cuñado N, Coriton O, et al. . 2014. Homoeologous chromosome sorting and progression of meiotic recombination in Brassica napus: ploidy does matter. Plant Cell 26: 1448–1463. PubMed PMC

Grant V. 1971. Plant speciation. New York: Columbia University Press.

Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.

Hemleben V, Kovařík A, Torres-Ruiz RA, Volkov RA, Beridze T. 2007. Plant highly repeated satellite DNA: molecular evolution, distribution and use for identification of hybrids. Systematics and Biodiversity 5: 277–289.

Henikoff S, Ahmad K, Malik HS. 2001. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293: 1098–1102. PubMed

Herklotz V, Kovařík A, Lunerová J, Lippitsch S, Groth M, Ritz CM. 2018. The fate of ribosomal RNA genes in spontaneous polyploid dogrose hybrids [Rosa L. sect. Caninae (DC.) Ser.] exhibiting non-symmetrical meiosis. Plant Journal 94: 77–90. PubMed

Herklotz V, Ritz CM. 2014. Spontane Hybridisierung von Hundsrosen (Rosa L. sect. Caninae (DC). Ser.) an einem natürlichen Vorkommen in der Oberlausitz (Sachsen, Deutschland). Peckiana 9: 1–12.

Herklotz V, Ritz CM. 2017. Multiple and asymmetric origin of polyploid dogrose hybrids (Rosa L. sect. Caninae (DC.) Ser.) involving unreduced gametes. Annals of Botany 120: 209–220. PubMed PMC

Hibrand Saint-Oyant L, Ruttink T, Hamama L, et al. . 2018. A high-quality genome sequence of Rosa chinensis to elucidate ornamental traits. Nature Plants 4: 473–484. PubMed PMC

Hirsch H, Zimmermann H, Ritz CM, et al. . 2011. Tracking the origin of invasive Rosa rubiginosa populations in Argentina. International Journal of Plant Sciences 172: 530–540.

Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. PubMed

Hwang YJ, Ju YH, Mancia FH, et al. . 2017. Localization of two types of ribosomal DNA using fluorescence in situ hybridization in five wild rose species. Flower Research Journal 253: 110–117.

Jang TS, Emadzade K, Parker J, et al. . 2013. Chromosomal diversification and karyotype evolution of diploids in the cytologically diverse genus Prospero (Hyacinthaceae). BMC Evolutionary Biology 13: art136, 1–17. PubMed PMC

Jukes TH, Cantor CR. 1969. Evolution of protein molecules. In Munro HN, ed. Mammalian protein metabolism. New York: Academic Press, 21–132.

Khaitová LC, Werlemark G, Kovariková A, Nybom H, Kovařík A. 2014. High penetrance of a pan-canina type rDNA family in intersection Rosa hybrids suggests strong selection of bivalent chromosomes in the section Caninae. Cytogenetic and Genome Research 143: 104–113. PubMed

Kirov IV, Khrustaleva LI, Van Laere K, Van Roy N. 2015. Molecular cytogenetics in the genus Rosa: current status and future perspectives. Acta Horticulturae 1087: 41–48.

Kirov IV, Kiseleva AV, Van Laere K, Van Roy N, Khrustaleva LI. 2017. Tandem repeats of Allium fistulosum associated with major chromosomal landmarks. Molecular Genetics and Genomics 292: 453–464. PubMed

Kirov I, Van Laere K, De Riek J, De Keyser E, Van Roy N, Khrustaleva L. 2014. Anchoring linkage groups of the Rosa genetic map to physical chromosomes with Tyramide-FISH and EST-SNP markers. PLoS One 9: e95793. PubMed PMC

Kirov IV, Van Laere K, Van Roy N, Khrustaleva LI. 2016. Towards a FISH-based karyotype of Rosa L. (Rosaceae). Comparative Cytogenetics 10: 543–554. PubMed PMC

Klemme S, Banaei-Moghaddam AM, Macas J, Wicker T, Novák P, Houben A. 2013. High-copy sequences reveal distinct evolution of the rye B chromosome. New Phytologist 199: 550–55 8. PubMed

Kolarčik V, Kocová V, Vašková D, . 2018. Flow cytometric seed screen data are consistent with models of chromosome inheritance in asymmetrically compensating allopolyploids. Cytometry Part A 93A: 737–748. PubMed

Koopman WJM, Wissemann V, De Cock K, et al. . 2008. AFLP markers as a tool to reconstruct complex relationships: a case study in Rosa (Rosaceae). American Journal of Botany 95: 353–366. PubMed

Kovařík A, Werlemark G, Leitch AR, et al. . 2008. The asymmetric meiosis in pentaploid dogroses (Rosa sect. Caninae) is associated with a skewed distribution of rRNA gene families in the gametes. Heredity 101: 359–67. PubMed

Kurrto A, Lampinen R, Junikka L. 2004. Atlas Florae Europaeae. Distribution of vascular plants in Europe. Helsinki: The Committee for Mapping the Flora of Europe & Societas Biologica Fennica Vanamo.

Lee YI, Yap JW, Izan S, et al. . 2018. Satellite DNA in Paphiopedilum subgenus Parvisepalum as revealed by high-throughput sequencing and fluorescent in situ hybridization. BMC Genomics 19: 578. PubMed PMC

Lewis WH, Bayse RE. 1961. Analysis of nine crosses between diploid Rosa species. Proceedings of American Society of Horticulture Science 78: 573–579.

Lim KY, Werlemark G, Matyášek R, et al. . 2005. Evolutionary implications of permanent odd polyploidy in the stable sexual, pentaploid of Rosa canina L. Heredity 94: 501–50 6. PubMed

Ma Y, IslamFaridi MN, Crane CF, et al. . 1997. In situ hybridization of ribosomal DNA to rose chromosomes. Journal of Heredity 88: 158–161.

Ma Y, IslamFaridi MN, Crane CF, Stelly DM, Price HJ, Byrne DH. 1996. A new procedure to prepare slides of metaphase chromosomes of roses. Hortscience 31: 855–857.

Macas J, Novák P, Pellicer J, et al. . 2015. In depth characterization of repetitive DNA in 23 plant genomes reveals sources of genome size variation in the legume tribe Fabeae. PLoS One 10: e0143424. PubMed PMC

Małecka J, Popek R. 1982. Karyological studies in the Polish representatives of the genus Rosa L. I. Acta Biologica Cracoviensia Series Botanica 14: 79–90.

Małecka J, Popek R. 1984. Karyological studies in the Polish representatives of the genus Rosa L. II. Acta Biologica Cracoviensia Series Botanica 16: 43–54.

Marques A, Klemme S, Houben A. 2018. Evolution of plant B chromosome enriched sequences. Genes (Basel) 9: E515. doi: 10.3390/genes9100515. PubMed DOI PMC

Mestrovic N, Mravinac B, Pavlek M, Vojvoda-Zeljko T, Satovic E, Plohl M. 2015. Structural and functional liaisons between transposable elements and satellite DNAs. Chromosome Research 23: 583–596. PubMed

Nakamura N, Hirakawa H, Sato S, et al. . 2018. Genome structure of Rosa multiflora, a wild ancestor of cultivated roses. DNA Research 25: 113–121. PubMed PMC

Novák 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. Bioinformatics 29: 792–793. PubMed

Novák P, Robledillo LA, Koblížková A, Vrbová I, Neumann P, Macas J. 2017. Tarean: a computational tool for identification and characterization of satellite DNA from unassembled short reads. Nucleic Acids Research 45: e111. PubMed PMC

Nybom H, Esselink GD, Werlemark G, Leus L, Vosman B. 2006. Unique genomic configuration revealed by microsatellite DNA in polyploid dogroses, Rosa sect. Caninae. Journal of Evolutionary Biology 19: 635–648. PubMed

Nybom H, Esselink GD, Werlemark G, Vosman B. 2004. Microsatellite DNA marker inheritance indicates preferential pairing between two highly homologous genomes in polyploid and hemisexual dog-roses, Rosa L. Sect. Caninae DC. Heredity 92: 139–50. PubMed

Pachl Š. 2011. Variablita botanických druhů rodu Rosa L., a možnosti jejich využití v krajinářské tvorbê. PhD Thesis, Slovak University of Agriculture, Nitra, Slovakia.

Pele A, Rousseau-Gueutin M, Chevre AM. 2018. Speciation success of polyploid plants closely relates to the regulation of meiotic recombination. Frontiers in Plant Science 9: 907. PubMed PMC

Pires JC, Lim KY, Kovařík A, et al. . 2004. Molecular cytogenetic analysis of recently evolved Tragopogon (Asteraceae) allopolyploids reveal a karyotype that is additive of the diploid progenitors. American Journal of Botany 91: 1022–1035. PubMed

Plohl M, Luchetti A, Mestrović N, Mantovani B. 2008. Satellite DNAs between selfishness and functionality: structure, genomics and evolution of tandem repeats in centromeric (hetero)chromatin. Gene 409: 72–82. PubMed

Price L, Short KC, Roberts AV. 1981. Poor resolution of C-bands and the presence of B-chromosomes in Rosa rugosa Scabrosa. Caryologia 34: 69–72.

Ramsey J, Schemske DW. 1998. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annual Review of Ecology and Systematics 29: 467–501.

Renny-Byfield S, Kovařík A, Chester M, et al. . 2012. Independent, rapid and targeted loss of highly repetitive DNA in natural and synthetic allopolyploids of Nicotiana tabacum. PLoS One 7: e36963. PubMed PMC

Ritz CM, Schmuths H, Wissemann V. 2005. Evolution by reticulation: European dogroses originated by multiple hybridization across the genus Rosa. Journal of Heredity 96: 4–14. PubMed

Ritz CM, Wissemann V. 2011. Microsatellite analyses of artificial and spontaneous dogrose hybrids reveal the hybridogenic origin of Rosa micrantha by the contribution of unreduced gametes. Journal of Heredity 102: 217–227. PubMed

Roberts AV, Gladis T, Brumme H. 2009. DNA amounts of roses (Rosa L.) and their use in attributing ploidy levels. Plant Cell Reports 28: 61–71. PubMed

Saint-Oyant LH, Ruttink T, Hamama L, et al. . 2018. A high-quality genome sequence of Rosa chinensis to elucidate ornamental traits. Nature Plants 4: 473–484. PubMed PMC

Schindelin J, Arganda-Carreras I, Frise E, et al. . 2012. Fiji: an open-source platform for biological-image analysis. Nature Methods 9: 676–682. PubMed PMC

Schwarzacher T, Heslop-Harrison P. 2000. Practical in situ hybridization. Oxford:BIOS Scientific Publishers.

Täckholm G. 1920. On the cytology of the genus Rosa. A preliminary note. Svensk Botanisk Tidskrift 14: 300–311.

Täckholm G. 1922. Zytologische Studien über die Gattung Rosa. Acta Horti Bergiani 7: 97–381.

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729. PubMed PMC

Teppner H. 1971. Cytosystematik, bimodale Chromosomensätze und permanente Anorthoploidie bei Onosma (Boraginaceae). Österreichische Botanische Zeitschrift 119: 196–233.

Van de Peer Y, Mizrachi E, Marchal K. 2017. The evolutionary significance of ancient genome duplications. Nature Reviews Genetics 18: 411–424. PubMed

Wendel JF. 2015. The wondrous cycles of polyploidy in plants. American Journal of Botany 102: 1753–1756. PubMed

Werlemark G, Nybom H. 2001. Skewed distribution of morphological character scores and molecular markers in three interspecific crosses in Rosa sect. Caninae. Hereditas 134: 1–13. PubMed

Wissemann V. 1999. Genetic constitution of Rosa sect. Caninae (R. canina, R. jundzilli) and sect. Gallicanae (R. gallica). Journal of Applied Botany 73: 191–196.

Wissemann V. 2002. Molecular evidence for allopolyploid origin of the Rosa canina-complex (Rosaceae, Rosoideae). Journal of Applied Botany 76: 176–178.

Wissemann V. 2003. Conventional taxonomy (wild roses). In: Roberts AV, Debener T, Gudin S, eds. Encyklopedia of rose science. Oxford: Elsevier Academic Press, 111–117.

Wissemann V, Ritz CM. 2005. The genus Rosa (Rosoideae, Rosaceae) revisited: molecular analysis of nrITS-1 and atpB-rbcL intergenic spacer (IGS) versus conventional taxonomy. Botanical Journal of the Linnean Society 147: 275–290.

Wulff HD. 1954. Über das spontane Auftreten einer Caninae-Meiosis bei der Mikrosporogenese der diploiden Rosa ruga Lindl. Oesterreichische Botanische Zeitschrift 101: 539–557.

Xiang YZ, Huang CH, Hu Y, et al. . 2017. Evolution of Rosaceae fruit types based on nuclear phylogeny in the context of geological times and genome duplication. Molecular Biology and Evolution 34: 1026. PubMed PMC

Zhang S-D, Jin J, Chen S-C, et al. . 2017. Diversification of Rosaceae since the Late Cretaceous based on plastid phylogenomics. New Phytologist 214: 1355–1367. PubMed

Zhang HQ, Koblížková A, Wang K, et al. . 2014. Boom–bust turnovers of megabase-sized centromeric DNA in Solanum species: rapid evolution of DNA sequences associated with centromeres. Plant Cell 26: 1436–1447. PubMed PMC

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

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)

Ancient Origin of Two 5S rDNA Families Dominating in the Genus Rosa and Their Behavior in the Canina-Type Meiosis