FIERY1 promotes microRNA accumulation by suppressing rRNA-derived small interfering RNAs in Arabidopsis

Chenjiang You,Xuemei Chen,Runlai Hang,Beixin Mo,Xiaofeng Cao,Wenrong He,Cuiju Zhang,Hongwei Guo,Jie Cui

doi:10.1038/s41467-019-12379-z

Abstract

Plant microRNAs (miRNAs) associate with ARGONAUTE1 (AGO1) to direct post-transcriptional gene silencing and regulate numerous biological processes. Although AGO1 predominantly binds miRNAs in vivo, it also associates with endogenous small interfering RNAs (siRNAs). It is unclear whether the miRNA/siRNA balance affects miRNA activities. Here we report that FIERY1 (FRY1), which is involved in 5′−3′ RNA degradation, regulates miRNA abundance and function by suppressing the biogenesis of ribosomal RNA-derived siRNAs (risiRNAs). In mutants of FRY1 and the nuclear 5′−3′ exonuclease genes XRN2 and XRN3, we find that a large number of 21-nt risiRNAs are generated through an endogenous siRNA biogenesis pathway. The production of risiRNAs correlates with pre-rRNA processing defects in these mutants. We also show that these risiRNAs are loaded into AGO1, causing reduced loading of miRNAs. This study reveals a previously unknown link between rRNA processing and miRNA accumulation.

Highlights

Plant microRNAs associate with ARGONAUTE1 (AGO1) to direct posttranscriptional gene silencing and regulate numerous biological processes
These risiRNAs can be loaded into NRDE-3, a nuclear Ago protein, and potentially target Ribosomal RNA (rRNA) precursors[19,20]
These small interfering RNAs (siRNAs) are not derived from rRNA precursors or mature rRNAs as they are generated in a Pol IV-dependent manner

Summary

Introduction

Plant microRNAs (miRNAs) associate with ARGONAUTE1 (AGO1) to direct posttranscriptional gene silencing and regulate numerous biological processes. AGO1 predominantly binds miRNAs in vivo, it associates with endogenous small interfering RNAs (siRNAs). We report that FIERY1 (FRY1), which is involved in 5′−3′ RNA degradation, regulates miRNA abundance and function by suppressing the biogenesis of ribosomal RNA-derived siRNAs (risiRNAs). MiRNA precursors are processed by DICERLIKE1 (DCL1) into mature miRNAs4, whereas siRNAs from transgenes, viruses, and endogenous transcripts are generated by other DCLs2,3,5,6 Both miRNAs and siRNAs undergo 3′ terminal methylation by HUA ENHANCER1 (HEN1)[7,8]. Both types of sRNAs associate with ARGONAUTE1 (AGO1) to form the functional RNA-induced silencing complex (RISC)[1,2,3]. A recent report found that viral infections trigger the production of siRNAs from rRNAs, but the molecular or biological impacts of these ribosomal small RNAs remain unknown[25]

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Conclusion