Ribosome stalling-induced NIP5;1 mRNA decay triggers ARGONAUTE1-dependent transcription downregulation

Tanaka, Mayuki, Sotta, Naoyuki ORCID: https://orcid.org/0000-0001-5558-5155, Duncan, Susan, Chiba, Yukako, Onouchi, Hitoshi, Marée, Athanasius F. M. ORCID: https://orcid.org/0000-0003-2689-2484, Naito, Satoshi, Grieneisen, Veronica A. ORCID: https://orcid.org/0000-0001-6780-8301 and Fujiwara, Toru 2025. Ribosome stalling-induced NIP5;1 mRNA decay triggers ARGONAUTE1-dependent transcription downregulation. Nucleic Acids Research 53 (5) 10.1093/nar/gkaf159

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Abstract

In eukaryotes, messenger RNA (mRNA) accumulation is regulated through the levels of transcription, processing, and degradation. Here, we unco v er the multi-le v el regulatory mechanism go v erning the e xpression of NIP5;1 , a boron (B) diffusion facilitator in Arabidopsis . B-dependent NIP5;1 mRNA degradation is triggered by ribosome stalling at an AUGUAA sequence in its 5'-untranslated region. We sho w ed that deletion of A TGT AA also abolishes B-dependent transcriptional do wnregulation, re v ealing a dual role of this sequence in both mRNA degradation and tran- scriptional control. Small RNAs (sRNAs) and ARGONAUTE1 (AGO1) are implicated in mRNA-degradation-mediated B-dependent transcriptional do wnregulation: a 5'–3' e x onuclease mutant, xrn4 , presents both ele v ated le v els of NIP5;1 mRNA degradation intermediates and transcriptional do wnregulation; AGO1-associated sRNA-sequencing re v eals the presence of sRNAs with sequences upstream of NIP5;1 AUGUAA; and nascent mRNA profiling by global run-on sequencing demonstrates RNA polymerase II pausing at A TGT AA, a phenomenon diminished in the ago1 mutant that lacks B-dependent transcriptional do wnregulation. T hese findings point to multi-le v el coordination of NIP5;1 expression with the AUGUAA sequence at its core: ribosome stalling orchestrates translational inhibition, mRNA degradation and transcriptional downregulation in response to B. The fast response resulting from this synergy suggests that similar mechanisms may exist in other eukaryotic systems for efficient and rapid regulation of gene expression.

Item Type:	Article
Date Type:	Publication
Status:	Published
Schools:	Schools > Biosciences
Publisher:	Oxford University Press
ISSN:	0305-1048
Date of First Compliant Deposit:	14 March 2025
Date of Acceptance:	18 February 2025
Last Modified:	21 Mar 2025 09:29
URI:	https://orca.cardiff.ac.uk/id/eprint/176893

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