Asymmetrical canina meiosis is accompanied by the expansion of a pericentromeric satellite in non-recombining univalent chromosomes in the genus Rosa

Abstract

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.

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

“…Interestingly, members of sect. Rosa tend to have much smaller loci of the centromeric satellite repeat CANR4 compared to other species of the genus ( Lunerova et al, 2020 ). However, R. nitida is exceptional in having large abundance of the CANR4 satellite (10 out 14 chromosomes carried strong FISH signals, not shown).…”

“…For the more distantly related species, Rosa spinosissima and R. persica , similarity threshold parameter was decreased to 80% (for the 5S_B variant). The genome abundance and copy number was calculated from genome proportions according to the formula stated in ( Lunerova et al, 2020 ).…”

“…Scale bar: 10 µm. Lunerova et al, 2020). Previous studies based on microsatellite markers revealed genetic distinction between bivalent-and univalent-forming chromosomes (Nybom et al, 2006).…”

“…Caninae ) by Rosa gallica and Rosa arvensis which perform regular meiosis ( Wissemann and Ritz, 2005 ; Fougere-Danezan et al, 2015 ). Thus, Canina meiosis has been probably evolved twice, which is supported by fluorescence in situ hybridization (FISH) analyses of meiotic chromosomes ( Herklotz et al, 2018 ; Lunerova et al, 2020 ).…”

“…c Q-5S families quantification by reads mapping, P-phylogeny tree construction, R-cluster analysis by RepeatExplorer, and F-fluorescent in situ hybridization. d Sequence read archives (ENA/NCBI) submitted as parts of original projects (Herklotz et al, 2018;Nakamura et al, 2018;Saint-Oyant et al, 2018;Lunerova et al, 2020).…”