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

Abstract

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.

Variation in Ribosomal DNA in the Genus Trifolium (Fabaceae)

“…Odd numbers of 5S rDNA loci were observed in T. glanduliferum ( Figure S6B and Figure 1 C) and T. alpestre ( Figure S2B and Figure 1 D), with 5 and 11 loci, respectively. Odd numbers of 5S rDNA loci have been observed also in Byblis , Tanacetum , and Rosa species [ 49 , 50 , 51 ], as have odd numbers of 35S rDNA loci in Fragaria [ 52 ].…”

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)

“…However, SNP-based analyses of ITS helped to investigate the origin of hybridogenic taxa ( Ritz et al, 2005 ; Herklotz et al, 2018 ; see below). The evolution of the 5S rDNA in roses turned out to be complex because two early diverged variants coexist in various amounts across the genus ( Vozárová et al, 2021 ). The pattern retrieved from the PCoA ( Figure 7C ) clearly reflects the proportion of A and B variants of 5S rDNA ( Vozárová et al, 2021 ), namely that dogroses contain higher proportions of the A variant, which is typical for the Rosa and allies clade compared to the B variant, which is overrepresented in the Synstylae and allies clade.…”

“…The evolution of the 5S rDNA in roses turned out to be complex because two early diverged variants coexist in various amounts across the genus ( Vozárová et al, 2021 ). The pattern retrieved from the PCoA ( Figure 7C ) clearly reflects the proportion of A and B variants of 5S rDNA ( Vozárová et al, 2021 ), namely that dogroses contain higher proportions of the A variant, which is typical for the Rosa and allies clade compared to the B variant, which is overrepresented in the Synstylae and allies clade. However, our comparative repeatome analysis of the 5S rDNA cluster in roses revealed more variants represented by at least four loops in the graphical display of the cluster ( Figure 6B ) and thus mixed signals of artificial recombination or several variants.…”

“…Caninae separated from subsect. Rubigineae and Vestitae ( Herklotz et al, 2018 ; Lunerová et al, 2020 ; Vozárová et al, 2021 ), all members are characterized by an asymmetric meiosis system, namely the Canina meiosis ( Blackburn and Harrison, 1921 ; Täckholm, 1922 ). During the course of this meiosis, only two subgenome form bivalents, whereas the other chromosome sets remain unpaired.…”

5S-IGS rDNA in wind-pollinated trees (FagusL.) encapsulates 55 million years of reticulate evolution and hybrid origins of modern species

“…The 5S intergenic spacers provide a unique source of information to investigate these multifaceted evolutionary processes (see also Volkov et al, 2017;Garcia et al, 2020;Vozárová et al, 2021). Despite our limited sample, our HTS data captured Quercus: Simeone et al, 2016;McVay et al, 2017;Hipp et al, 2020;Nothofagus: Premoli et al, 2012;Acosta & Premoli, 2018).…”