Abstract
In eukaryotic cells, ribosomal RNAs (rRNAs) are transcribed, processed, and assembled with ribosomal proteins in the nucleolus. Regulatory mechanisms of rRNA gene (rDNA) transcription and processing remain elusive in plants, especially their connection to nucleolar organization. We performed an in silico screen for essential genes of unknown function in Arabidopsis thaliana and identified Thallo (THAL) encoding a SAS10/C1D family protein. THAL disruption caused enlarged nucleoli in arrested embryos, aberrant processing of precursor rRNAs at the 5’ External Transcribed Spacer, and repression of the major rDNA variant (VAR1). THAL overexpression lines showed de-repression of VAR1 and overall reversed effects on rRNA processing sites. Strikingly, THAL overexpression also induced formation of multiple nucleoli per nucleus phenotypic of mutants of heterochromatin factors. THAL physically associated with histone chaperone Nucleolin 1 (NUC1), histone-binding NUC2, and histone demethylase Jumonji 14 (JMJ14) in bimolecular fluorescence complementation assay, suggesting that it participates in chromatin regulation. Furthermore, investigation of truncated THAL proteins revealed that the SAS10 C-terminal domain is likely important for its function in chromatin configuration. THAL also interacted with putative Small Subunit processome components, including previously unreported Arabidopsis homologue of yeast M Phase Phosphoprotein 10 (MPP10). Our results uncovering the dual role of THAL in transcription and processing events critical for proper rRNA biogenesis and nucleolar organization during reproduction are the first to define the function of SAS10/C1D family members in plants.
Highlights
The biogenesis of mature 5.8S, 18S, and 25S ribosomal RNAs requires transcription of 45S rRNA genes and processing of 45S precursor rRNAs in the nucleolus [1]
We identified a previously uncharacterized Something About Silencing 10 (SAS10)/C1D family protein
The nucleolus is not enclosed by a membrane; its formation is driven by the active transcription of rDNA and structured by pre-rRNA processing and ribosome assembly components. rDNA units are tandemly arrayed at nucleolar organizer regions (NORs), and NORs of Arabidopsis thaliana (Arabidopsis) abut upon the northern telomeres of chromosomes 2 and 4 (NOR2 and NOR4, [2])
Summary
The biogenesis of mature 5.8S, 18S, and 25S ribosomal RNAs (rRNAs) requires transcription of 45S rRNA genes (rDNA) and processing of 45S precursor rRNAs (pre-rRNAs) in the nucleolus [1]. The nucleolus is not enclosed by a membrane; its formation is driven by the active transcription of rDNA and structured by pre-rRNA processing and ribosome assembly components. One major component in the nucleolus is the Small Subunit (SSU) processome, a ribonucleoprotein (RNP) complex required for biogenesis of 18S rRNA and subsequent assembly and maturation of the ribosome SSU in yeast Saccharomyces cerevisiae [5]. It contains the U3 small nucleolar RNA (snoRNA) and U Three Proteins (UTPs), with a total of as many as 72 nonribosomal proteins which compose numerous subcomplexes [6]. Extensively studied in yeast, the SSU processome is not validated in many other organisms including Arabidopsis
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