Concerted Evolution of rDNA in Recently Formed Tragopogon Allotetraploids Is Typically Associated With an Inverse Correlation Between Gene Copy Number and Expression

Abstract

We analyzed nuclear ribosomal DNA (rDNA) transcription and chromatin condensation in individuals from several populations of Tragopogon mirus and T. miscellus, allotetraploids that have formed repeatedly within only the last 80 years from T. dubius and T. porrifolius and T. dubius and T. pratensis, respectively. We identified populations with no (2), partial (2), and complete (4) nucleolar dominance. It is probable that epigenetic regulation following allopolyploidization varies between populations, with a tendency toward nucleolar dominance by one parental homeologue. Dominant rDNA loci are largely decondensed at interphase while silent loci formed condensed heterochromatic regions excluded from nucleoli. Those populations where nucleolar dominance is fixed are epigenetically more stable than those with partial or incomplete dominance. Previous studies indicated that concerted evolution has partially homogenized thousands of parental rDNA units typically reducing the copy numbers of those derived from the T. dubius diploid parent. Paradoxically, despite their low copy number, repeats of T. dubius origin dominate rDNA transcription in most populations studied, i.e., rDNA units that are genetic losers (copy numbers) are epigenetic winners (high expression). E PIGENETIC silencing of parental genes is an important feature of newly established allopolyploids and is believed to reconcile regulatory incompatibilities between parental subgenomes (Adams and Wendel 2005;Birchler et al., 2005). Nucleolus organizer regions (NORs) contain tandemly arranged highly reiterated ribosomal rRNA genes coding for 18S-5.8S-26S rRNA whose expression is under epigenetic control (Pikaard 2000; for review see Neves et al. 2005). Indeed nucleolar dominance (ND) was one of the first examples of differential gene expression discovered in plant hybrids nearly a century ago (Navashin 1934). Numerous studies in both plants and animals support the view that ND/rRNA gene silencing may be stable or unstable, partial, or reversible (Volkov et al. 2007). In Arabidopsis and Brassica biochemical (Chen and Pikaard 1997a) and genetic (Lawrence et al. 2004;Probst et al. 2004) studies provided evidence that rRNA silencing depends on epigenetic factors, including DNA methylation and histone acetylation (for review see Preuss and Pikaard 2007). Other factors may also play a role in ND, e.g., the position of rRNA genes in the nucleus (Shaw and Jordan 1995), the relative amount of heterochromatin (Viegas et al. 2002), and the activity of unlinked genes . Despite considerable progress in our understanding of ND, little is known about the relationship between ND and sequence homogenization, particularly in young populations of newly formed polyploidy species. The goal of this article is to study this relationship and the inheritance patterns of ND and sequence homogenization at individual and population levels in recently formed allotetraploid species.Besides epigenetic silencing homogenization of repeats seems to be another interesting aspect of rDNA...

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)

“…A noteworthy fact is that even minor families may be highly transcriptionally active as indicated by enhanced signals in CAPS analysis (Figure 3b, panel R. sherardii and Figure 3c, panel R. dumalis). The phenomenon of low-copy gene-family expression dominance has also been observed in other allopolyploid systems (Joly et al, 2004;Matyasek et al, 2007). With all evidence taken together, it seems that the b-family, residing on bivalent-forming genomes (Kovarik et al, 2008b) is stably expressed across the species, whereas families residing on univalent genomes tend to be suppressed.…”

Characterization of Eu- and Heterochromatin of <i>Citrus</i> with a Focus on the Condensation Behavior of 45S rDNA Chromatin

“…In many plant hybrids, only one parental set of rRNA genes retains the ability for nucleolus formation, while the nucleolus organizer regions (NORs) of the other species are silent. Such nucleolar dominance is frequently observed in allopolyploid species [Lawrence et al, 2004;Neves et al, 2005;Matyasek et al, 2007]. Considering that the same phenomenon might also occur in Citrus , it is possible that the different condensation degrees of the 45S rDNA sites found are caused by nucleolar dominance.…”

Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids

“…Perhaps polyploidy in T. miscellus sets the stage for noninstantaneous, yet rapid, mutational mechanisms that are ongoing through many generations. The most obvious of these is homoeologous recombination, in which fragments of chromosomes can be lost, though we cannot exclude the possibility of gene conversion, as has been found for rRNA genes in the species (Kovarik et al, 2005;Matyasek et al, 2007). Homoeologous recombination seems to have caused loss of chromosome fragments in re-synthesised Brassica allopolyploids (Song et al, 1995;Gaeta et al, 2007).…”