Abstract
In eukaryotes, 45S rRNA genes are arranged in tandem arrays in copy numbers ranging from several hundred to several thousand in plants. Although it is clear that not all copies are transcribed under normal growth conditions, the molecular basis controlling the expression of specific sets of rRNA genes remains unclear. Here, we report four major rRNA gene variants in Arabidopsis thaliana. Interestingly, while transcription of one of these rRNA variants is induced, the others are either repressed or remain unaltered in A. thaliana plants with a disrupted nucleolin-like protein gene (Atnuc-L1). Remarkably, the most highly represented rRNA gene variant, which is inactive in WT plants, is reactivated in Atnuc-L1 mutants. We show that accumulated pre–rRNAs originate from RNA Pol I transcription and are processed accurately. Moreover, we show that disruption of the AtNUC-L1 gene induces loss of symmetrical DNA methylation without affecting histone epigenetic marks at rRNA genes. Collectively, these data reveal a novel mechanism for rRNA gene transcriptional regulation in which the nucleolin protein plays a major role in controlling active and repressed rRNA gene variants in Arabidopsis.
Highlights
In eukaryotic cells, ribosomal RNA genes are arranged in head-to-tail tandem arrays
A linker histone H1 directs the path of DNA between adjacent nucleosomes to form the chromatin fiber
Chromatin compaction depends on DNA methylation and on a number of histone modifications, including methylation and acetylation of histone tails
Summary
Each rRNA gene transcription unit consists of sequences encoding a precursor transcript that includes the structural rRNAs (18S, 5.8S, 25S), the Internal Transcribed Spacers (ITS) and the External Transcribed Spacers (ETS). IGS organization in plant rRNA genes resembles IGS organization in most higher eukaryotes, including at least one array of tandemlyrepeated sequences located upstream from the transcription initiation site (TIS). In Xenopus [7] and mouse [8], repeated sequences in this location have been shown to possess enhancer activity, increasing the expression of the adjacent promoter after injection into frog oocytes or embryos or after transfection into cultured cells. Though Arabidopsis spacer repeats cloned next to a Xenopus rRNA gene promoter act as enhancers in frog oocytes [9], there is no evidence that they have analogous enhancer activity in plant cells [10]. Questions persist as to whether or not IGS heterogeneity affects rRNA transcription; possibly playing a role in activation or silencing of rRNA genes or in stimulating rRNA transcription levels among active rRNA genes
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