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

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 speci...

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Main Authors: Radka Vozárová, Veit Herklotz, Aleš Kovařík, Yuri O. Tynkevich, Roman A. Volkov, Christiane M. Ritz, Jana Lunerová
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-03-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.643548/full
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spelling doaj-e576b0f2a6514605b269ef7e69f6e9052021-03-08T16:43:14ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-03-011210.3389/fpls.2021.643548643548Ancient Origin of Two 5S rDNA Families Dominating in the Genus Rosa and Their Behavior in the Canina-Type MeiosisRadka Vozárová0Radka Vozárová1Veit Herklotz2Aleš Kovařík3Yuri O. Tynkevich4Roman A. Volkov5Christiane M. Ritz6Christiane M. Ritz7Jana Lunerová8Department of Molecular Epigenetics, Institute of Biophysics, Academy of Sciences of the Czech Republic, Brno, CzechiaDepartment of Experimental Biology, Faculty of Science, Masaryk University, Brno, CzechiaDepartment of Botany, Senckenberg Museum of Natural History Görlitz, Görlitz, GermanyDepartment of Molecular Epigenetics, Institute of Biophysics, Academy of Sciences of the Czech Republic, Brno, CzechiaDepartment of Molecular Genetics and Biotechnology, Yuriy Fedkovych Chernivtsi National University, Chernivtsi, UkraineDepartment of Molecular Genetics and Biotechnology, Yuriy Fedkovych Chernivtsi National University, Chernivtsi, UkraineDepartment of Botany, Senckenberg Museum of Natural History Görlitz, Görlitz, GermanyChair of Biodiversity of Higher Plants, International Institute (IHI) Zittau, Technische Universität Dresden, Zittau, GermanyDepartment of Molecular Epigenetics, Institute of Biophysics, Academy of Sciences of the Czech Republic, Brno, CzechiaThe 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.https://www.frontiersin.org/articles/10.3389/fpls.2021.643548/full5S rDNAevolutionRosagenomicscytogeneticsrepeatome
collection DOAJ
language English
format Article
sources DOAJ
author Radka Vozárová
Radka Vozárová
Veit Herklotz
Aleš Kovařík
Yuri O. Tynkevich
Roman A. Volkov
Christiane M. Ritz
Christiane M. Ritz
Jana Lunerová
spellingShingle Radka Vozárová
Radka Vozárová
Veit Herklotz
Aleš Kovařík
Yuri O. Tynkevich
Roman A. Volkov
Christiane M. Ritz
Christiane M. Ritz
Jana Lunerová
Ancient Origin of Two 5S rDNA Families Dominating in the Genus Rosa and Their Behavior in the Canina-Type Meiosis
Frontiers in Plant Science
5S rDNA
evolution
Rosa
genomics
cytogenetics
repeatome
author_facet Radka Vozárová
Radka Vozárová
Veit Herklotz
Aleš Kovařík
Yuri O. Tynkevich
Roman A. Volkov
Christiane M. Ritz
Christiane M. Ritz
Jana Lunerová
author_sort Radka Vozárová
title Ancient Origin of Two 5S rDNA Families Dominating in the Genus Rosa and Their Behavior in the Canina-Type Meiosis
title_short Ancient Origin of Two 5S rDNA Families Dominating in the Genus Rosa and Their Behavior in the Canina-Type Meiosis
title_full Ancient Origin of Two 5S rDNA Families Dominating in the Genus Rosa and Their Behavior in the Canina-Type Meiosis
title_fullStr Ancient Origin of Two 5S rDNA Families Dominating in the Genus Rosa and Their Behavior in the Canina-Type Meiosis
title_full_unstemmed Ancient Origin of Two 5S rDNA Families Dominating in the Genus Rosa and Their Behavior in the Canina-Type Meiosis
title_sort ancient origin of two 5s rdna families dominating in the genus rosa and their behavior in the canina-type meiosis
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2021-03-01
description 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.
topic 5S rDNA
evolution
Rosa
genomics
cytogenetics
repeatome
url https://www.frontiersin.org/articles/10.3389/fpls.2021.643548/full
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