Epistatic and allelic interactions control expression of ribosomal RNA gene clusters in Arabidopsis thaliana

Abstract

BackgroundRibosomal RNA (rRNA) accounts for the majority of the RNA in eukaryotic cells, and is encoded by hundreds to thousands of nearly identical gene copies, only a subset of which are active at any given time. In Arabidopsis thaliana, 45S rRNA genes are found in two large ribosomal DNA (rDNA) clusters and little is known about the contribution of each to the overall transcription pattern in the species.ResultsBy taking advantage of genome sequencing data from the 1001 Genomes Consortium, we characterize rRNA gene sequence variation within and among accessions. Notably, variation is not restricted to the pre-rRNA sequences removed during processing, but it is also present within the highly conserved ribosomal subunits. Through linkage mapping we assign these variants to a particular rDNA cluster unambiguously and use them as reporters of rDNA cluster-specific expression. We demonstrate that rDNA cluster-usage varies greatly among accessions and that rDNA cluster-specific expression and silencing is controlled via genetic interactions between entire rDNA cluster haplotypes (alleles).ConclusionsWe show that rRNA gene cluster expression is controlled via complex epistatic and allelic interactions between rDNA haplotypes that apparently regulate the entire rRNA gene cluster. Furthermore, the sequence polymorphism we discovered implies that the pool of rRNA in a cell may be heterogeneous, which could have functional consequences.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-017-1209-z) contains supplementary material, which is available to authorized users.

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

“…Such a distribution pattern of SNPs in the rDNA units has also been observed in other organisms, e.g. A. thaliana (Rabanal et al, 2017), Nicotiana species (Lunerova et al, 2017), some mosses (Liu et al, 2013;Rosato et al, 2016) and some fungi (Ganley and Kobayashi, 2007). Interestingly, we detected a higher number of SNPs and increased ITS1 diversity in B. stacei rDNA than in B. distachyon rDNA (both genotypes).…”

Regulation of Nucleolar Dominance in Drosophila melanogaster

“…These results suggest that Y rDNA and/or its proximal region within YS carries critical information that allows for establishment of nucleolar dominance, where Y rDNA is transcribed and X rDNA is silenced. This is similar to what has been seen in Arabidopsis, where nucleolar dominance is "allelic" and possibly influenced by rDNA sequence differences (Rabanal et al 2017). Additionally, the observation that the degree of Y rDNA dominance in Xbb 2 YS/X females is much less than that in X/Y males or C(1)RM/Y females indicates that the chromosomal context (Chandrasekhara et al 2016) (e.g., being embedded in the entire Y chromosome) and/or with other factor(s) on the long arm of the Y chromosome (YL) also play a role in the determination of Y rDNA dominance (see Discussion).…”

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