Frequent silencing of rDNA loci on the univalent-forming genomes contrasts with their stable expression on the bivalent-forming genomes in polyploid dogroses (Rosa sect. Caninae)

Abstract

The polyploid species in Rosa section Caninae (2n ¼ 21, 28 or 35) are characterized by an unusual reproductive system known as odd (or asymmetric) meiosis. Only two chromosome sets form bivalents in meiosis, whereas the remaining chromosomes are transmitted as univalents through the female germline. Evolution of ribosomal rRNA genes (rDNA) does not seem to be significantly affected by interlocus homogenization in dogroses. As a consequence, most species contain several rDNA families falling into two main clades (b and g) thought to be differentially distributed between bivalent and univalent chromosomes, respectively. Here, we have investigated expression of rRNA gene families in five pentaploid species (R. canina, R. rubiginosa, R. dumalis, R. sherardii and R. caesia, 2n ¼ 35) and in one tetraploid (R. mollis, 2n ¼ 28). Using extensive sequencing of ITS clones and cleaved amplified polymorphism sequence (CAPS) analysis, we found that the b-family was constitutively expressed in all species. However, there was large variation in the expression patterns of families constituting the g-clade. In addition, a single family can be active in one species, whereas silenced in another. The data show that the families on bivalent-forming chromosomes dominate rDNA expression in all dogrose species. We hypothesize that genes on bivalent genomes are stably expressed, whereas those on univalent genomes undergo variable levels of epigenetic silencing. Nonetheless, mosaic expression of univalent genomes could contribute to phenotypic variation between the species.

Comparative Characterization of Ribosomal DNA Regions in Different Agave Accessions with Economical Importance

“…Interestingly, the species more highly cultivated and with major non-redundant haplotypes, A. tequilana Weber, exhibits a similar total expression profile for both rDNA genes, implying a strong regulation of 5S rDNA under the 18S rDNA. This is similar to previous reports for several important crops such as tobacco, wheat, and rose (Flavell et al 1986;Dadejová et al 2007;Kovarik et al 2008;Khaitová et al 2010). Two important observations help us to support a more detailed rDNA expression analysis in the more regulated 5S rDNA gene.…”

Genomic aspects of research involving polyploid plants

“…The mechanism of this gene silencing was unknown. Recently, Khaitova et al (2010) investigated expression of rRNA gene families in five pentaploid dogrose species (Rosa canina, R. rubiginosa, R. dumalis, R. sherardii and R. caesia) and in one tetraploid species (R. mollis). Their data showed that the families occurring on bivalent-forming chromosomes dominated rDNA expression in all dogrose species, suggesting that genes on bivalent genomes were stably expressed, whereas those on univalent genomes underwent variable levels of epigenetic silencing.…”

High Penetrance of a Pan-<b><i>Canina</i></b> Type rDNA Family in Intersection <b><i>Rosa</i></b> Hybrids Suggests Strong Selection of Bivalent Chromosomes in the Section <b><i>Caninae</i></b>

“…Interestingly, heterogeneity of the 'André Brichet' ITS pool was comparable or even higher than in R. rubiginosa . This is not surprising, since both tetraploid and diploid rose species apparently contain several different ITS types [Iwata et al, 2000;Khaitova et al, 2010]. It seems that a relatively low homogenization pressure is not limited to the section Caninae but may operate across the whole genus.…”

“…The molecular nature of these rearrangements is unknown, but homeologous pairing [Szadkowski et al, 2010;Xiong et al, 2011] and epigenetic factors influencing chromatin configuration have been proposed [Ge et al, 2013;Kovarik et al, 2008b]. The gamma family already silenced in parental rose plants [Khaitova et al, 2010] could be epigenetically modified.…”

“…The beta family corresponds to the proto-canina type (C-type according to Wissemann [2003b]). This family is transcriptionally dominant while the gamma family is partially suppressed despite its high copy number [Khaitova et al, 2010]. To study the chromosomal location and meiotic transmission of individual rDNA families, we constructed intersection hybrids involving R. rubiginosa as a maternal parent and a garden rose R. hybrida 'André Brichet' (although hybridogenous, garden roses are usually treated within section Gallicanae ) as a paternal parent.…”