Epigenetics of the preferential silencing of Brachypodium stacei-originated 35S rDNA loci in the allotetraploid grass Brachypodium hybridum

Abstract

Nucleolar dominance (ND), initially described as ‘differential amphiplasty’, is a phenomenon observed in some plant and animal allopolyploids and hybrids in which the selective suppression of the activity of 35S rRNA gene loci that have been inherited from one of the two or more ancestral genomes occurs. Although more than 80 years have passed since the discovery of ND, there is still a significant lack in our understanding of the mechanisms that determine this phenomenon. Here, we aimed to investigate the epigenetic status of 35S rRNA gene loci in the monocotyledonous Brachypodium hybridum, which is an allotetraploid that has resulted from a cross between B. distachyon and B. stacei. We revealed that the repressed B. stacei-inherited rDNA loci are characterised by a high level of DNA methylation. The global hypomethylation of B. hybridum nuclear DNA induced by 5-azacytidine, however, seems to be insufficient for the transcriptional reactivation of these loci, which indicates that factors other than DNA methylation are behind the suppression of B. stacei-originated loci. We also showed that the transcriptionally active and silenced fractions of rRNA genes that had been inherited from B. distachyon occupy different domains within the chromocentres adjacent to the nucleolus, depending on their epigenetic status.

Chromosome identification and reconstruction of evolutionary rearrangements in Brachypodium distachyon, B. stacei and B. hybridum

“…1F ), is connected with the occurrence of nucleolar dominance in this genotype of B. hybridum . This enigmatic phenomenon results in the expression of only the 18S-5.8S-25S rRNA genes inherited from the B. distachyon progenitor ( Idziak and Hasterok, 2008 ; Borowska-Zuchowska et al , 2016 ; Borowska-Zuchowska and Hasterok, 2017 ).…”

“…Many cytological features and existing resources make B. distachyon and other species in the genus exceptionally useful model systems in various areas of plant molecular cytogenetics (e.g. Wolny et al , 2014 ; Idziak et al , 2015 ; Borowska-Zuchowska and Hasterok, 2017 ; Kus et al , 2017 ). The availability of the whole genome sequence of B. distachyon ( IBI, 2010 ) and its combination ( Febrer et al , 2010 ) with efficient BAC–FISH-based methodology ( Hasterok et al ., 2006 a , b ; Jenkins and Hasterok, 2007 ) enabled the first true chromosome painting in monocotyledonous plants ( Idziak et al , 2011 ; Betekhtin et al , 2014 ; Robaszkiewicz et al , 2016 ).…”

The fate of 35S rRNA genes in the allotetraploid grass Brachypodium hybridum

“…In contrast, the B. stacei-like rRNA genes were characterized by a high level of DNA methylation and were enriched with a heterochromatic marker: the dimethylated lysine 9 of histone H3 (H3K9me2). Interestingly, the global cytosine hypomethylation of the B. hybridum genome induced by 5-azacytidine did not lead to a reactivation of the S-genome rDNA loci, which strongly suggests the involvement of other factors that lie behind ND in this species (Borowska-Zuchowska and Hasterok, 2017).…”

“…We have previously used molecular cytogenetic approaches to study the epigenetic status of 35S rDNA loci in B. hybridum. The actively transcribed D-genome 35S rDNA units exhibited a low DNA methylation level and were enriched in euchromatic marks, such as acetylated histone isoforms (H4K5ac, H4K16ac and H3K9ac) (Borowska-Zuchowska and Hasterok, 2017). In contrast, the B. stacei-like rRNA genes were characterized by a high level of DNA methylation and were enriched with a heterochromatic marker: the dimethylated lysine 9 of histone H3 (H3K9me2).…”

The Utility of Graph Clustering of 5S Ribosomal DNA Homoeologs in Plant Allopolyploids, Homoploid Hybrids, and Cryptic Introgressants

“…We investigated rDNAs in two relatively ancient (c.1 Myr) allopolyploid systems (Gossypium and Brachypodium) which already show substantial loss of 35S rDNA homoeologous units (Wendel et al, 1995a;Borowska-Zuchowska and Hasterok, 2017). Gossypium allotetraploids were represented by five species with a typical AADD genome composition originating from common diploid ancestors closely related to G. arboreum (A genome) and G. raimondii (D genome).…”