Multiple epigenetic layers accompany the spatial distribution of ribosomal genes in Arabidopsis

45S ribosomal genes in A. thaliana (rDNA) are located in tandem arrays on termini of chromosomes 2 and 4 (NOR2 and NOR4) and encode rRNA, crucial structural elements of the ribosome. Inactive rDNA genes accumulate in the condensed chromocenters in the nucleus and at the nucleolar periphery, while nucleolus delimits the active genes. We show that a subset of nucleolar rDNA assembles into condensed foci marked by H3.1 and H3.3 histones and that progressive rDNA condensation is connected with rDNA transcriptional activity, cell ploidy and rDNA copy number. Interestingly, some nucleolar foci are reminiscent of perinucleolar chromocenters, containing the NOR4 region. We further demonstrate that rDNA promoter is a key regulatory region of the rDNA repeat and describe large involvement of repressive epigenetic mark H3K9me2 and H2A.W histone variant in rDNA activity regulation. In addition, we found euchromatic H3.3 histone enrichment at the rDNA transcription start site in actively dividing tissues, despite its accumulation in nucleolar foci containing condensed rDNA repeats.