Rumex acetosa is a dioecious plant with the XY1Y2 sex chromosome system. Both Y chromosomes are heterochromatic and are thought to be degenerated. We performed low-pass 454 sequencing and similarity-based clustering of male and female genomic 454 reads to identify and characterize major groups of R. acetosa repetitive DNA. We found that Copia and Gypsy retrotransposons dominated, followed by DNA transposons and nonlong terminal repeat retrotransposons. CRM and Tat/Ogre retrotransposons dominated the Gypsy superfamily, whereas Maximus/Sireviruses were most abundant among Copia retrotransposons. Only one Gypsy subfamily had accumulated on Y1 and Y2 chromosomes, whereas many retrotransposons were ubiquitous on autosomes and the X chromosome, but absent on Y1 and Y2 chromosomes, and others were depleted from the X chromosome. One group of CRM Gypsy was specifically localized to centromeres. We also found that majority of previously described satellites (RAYSI, RAYSII, RAYSIII, and RAE180) are accumulated on the Y chromosomes where we identified Y chromosome-specific variant of RAE180. We discovered two novel satellites—RA160 satellite dominating on the X chromosome and RA690 localized mostly on the Y1 chromosome. The expression pattern obtained from Illumina RNA sequencing showed that the expression of transposable elements is similar in leaves of both sexes and that satellites are also expressed. Contrasting patterns of transposable elements (TEs) and satellite localization on sex chromosomes in R. acetosa, where not only accumulation but also depletion of repetitive DNA was observed, suggest that a plethora of evolutionary processes can shape sex chromosomes.

Sex chromosomes are an ideal system to study processes connected with suppressed recombination. We found evidence of microsatellite expansion, on the relatively young Y chromosome of the dioecious plant sorrel (Rumex acetosa, XY1Y2 system), but no such expansion on the more ancient Y chromosomes of liverwort (Marchantia polymorpha) and human. The most expanding motifs were AC and AAC, which also showed periodicity of array length, indicating the importance of beginnings and ends of arrays. Our data indicate that abundance of microsatellites in genomes depends on the inherent expansion potential of specific motifs, which could be related to their stability and ability to adopt unusual DNA conformations. We also found that the abundance of microsatellites is higher in the neighborhood of transposable elements (TEs) suggesting that microsatellites are probably targets for TE insertions. This evidence suggests that microsatellite expansion is an early event shaping the Y chromosome where this process is not opposed by recombination, while accumulation of TEs and chromosome shrinkage predominate later.