Interpopulation hybridization generates meiotically stable rDNA epigenetic variants in allotetraploid Tragopogon mirus

Abstract

SUMMARYUniparental silencing of 35S rRNA genes (rDNA), known as nucleolar dominance (ND), is common in interspecific hybrids. Allotetraploid Tragopogon mirus composed of Tragopogon dubius (d) and Tragopogon porrifolius (p) genomes shows highly variable ND. To examine the molecular basis of such variation, we studied the genetic and epigenetic features of rDNA homeologs in several lines derived from recently and independently formed natural populations. Inbred lines derived from T. mirus with a dominant d-rDNA homeolog transmitted this expression pattern over generations, which may explain why it is prevalent among natural populations. In contrast, lines derived from the p-rDNA dominant progenitor were meiotically unstable, frequently switching to co-dominance. Interpopulation crosses between progenitors displaying reciprocal ND resulted in d-rDNA dominance, indicating immediate suppression of p-homeologs in F 1 hybrids. Original p-rDNA dominance was not restored in later generations, even in those segregants that inherited the corresponding parental rDNA genotype, thus indicating the generation of additional p-rDNA and d-rDNA epigenetic variants. Despite preserved intergenic spacer (IGS) structure, they showed altered cytosine methylation and chromatin condensation patterns, and a correlation between expression, hypomethylation of RNA Pol I promoters and chromatin decondensation was apparent. Reversion of such epigenetic variants occurred rarely, resulting in co-dominance maintained in individuals with distinct genotypes. Generally, interpopulation crosses may generate epialleles that are not present in natural populations, underlying epigenetic dynamics in young allopolyploids. We hypothesize that highly expressed variants with distinct IGS features may induce heritable epigenetic reprogramming of the partner rDNA arrays, harmonizing the expression of thousands of genes in allopolyploids.

Evolutional dynamics of 45S and 5S ribosomal DNA in ancient allohexaploid Atropa belladonna

“…This issue was originally described as nucleolar dominance (ND) by Navashin [65], and it was demonstrated later that at the molecular level ND means transcriptional silencing of 45S rDNA due to siRNA mediated differential methylation of cytosine, post-transcriptional modification of histone proteins and chromatin remodelling [13, 15, 27, 28, 30, 66]. It was also argued that differential activity of 45S rDNA in hybrids can be controlled by structural peculiarities of parental rDNA repeats (especially by that of IGS).…”

“…Later, it was also shown that in Vigna [69] and Solanum [27] the 45S rDNA repeats bearing more subrepeats down-stream of TIS appear to be more transcriptionally active. If no down-stream subrepeats are present in 45S rDNA, the variants possessing more subrepeats up-stream of TIS seem to be dominant (for review see [10, 13, 15, 26]). Considering these data, it is possible to suppose that four highly active sites of Atropa contain the long variant of 45S rDNA repeats, whereas the other two loci harbour the short one.…”

“…In contrast to the majority of repeated sequences, whose functions mostly remain unclear, activities of 5S and 45S rDNA genes are vital for organisms, providing rRNA species necessary for assembly of functional ribosomes, which account for more than 90% of total cellular RNA. In eukaryotes, the copy number (CN) of rDNA repeats is higher than is required for rRNA synthesis, and the redundant copies of rDNA are transcriptionally silenced [10, 13–15]. Transcriptionally active 45S rDNA loci (also known as nucleolus organizer regions, NORs) can be recognized by cytological chromosome analysis.…”

“…This is especially true for species of hybrid origin (for review see [10, 26]), where the inheritance and evolution of rDNA can follow various scenarios. Often in the first generation hybrids, the 45S rDNA loci inherited from both parents remain structurally intact while enduring differential transcriptional silencing [13, 15, 27–30]. In ancient allopolyploid species, a more complicated picture is usually observed with uniparental inheritance and/or structural rearrangements of parental 45S rDNA.…”

Ribosomal DNA loci derived fromBrachypodium staceiare switched off for major parts of the life cycle ofBrachypodium hybridum

“…It was demonstrated that the level of DNA methylation, especially in the PolI promoter sites, directly correlates with the expression of 35S rRNA genes. The actively transcribed rDNA units are hypomethylated, as has been reported for Brassica (Ksiazczyk et al ., 2011), wheat (Carvalho et al , 2010), Solanum (Komarova et al , 2004) and Tragopogon (Dobesova et al ., 2015; Matyasek et al , 2016) species. For instance, in the allotetraploid Tragopogon mirus (genomes DDPP), which has a homozygous macrodeletion of the majority of the D genome-originated 35S rDNA repeats, it was observed that the underdominant P genome-like rDNA units were reactivated.…”