Academic journal article Genetics

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

Academic journal article Genetics

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

Article excerpt

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).

EPIGENETIC 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 (LEWIS et al. 2004). 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 biology. The consequence of homogenization is little sequence variability among the units within and across the arrays in genome. In many allopolyploids' rDNA one particular unit overwrites preexisting units, probably mediated by recombination or copy number expansion/contraction mechanism that leads to the fast evolution of novel families, a process called concerted evolution (for review see ALVAREZ and WENDEL, 2003; VOLKOV et al. 2007).However, the frequency/occurrence of homogenization does vary between species. Allopolyploids of Arabidopsis and Brassica apparently have no rDNA unit loss or concerted evolution, despite an evolutionary history lasting several thousands of generations (BENNETT and SMITH 1991; O'KANE et al. 1996). In contrast studies in some recently formed allopolyploids (KOVARIK et al. 2005), synthetic interspecific hybrids and polyploids (LIN et al. 1985; CLUSTER et al. …

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