Arabidopsis SGS3 is recruited to chromatin by CHR11 to select RNA that initiate siRNA production

Taline Elmayan, Thomas Blein, Emilie Elvira-Matelot, Ivan Le Masson, Aurélie Christ, Nathalie Bouteiller, Martin D. Crespi and Hervé Vaucheret ()
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Taline Elmayan: Institut Jean-Pierre Bourgin for Plant Sciences (IJPB)
Thomas Blein: IPS2
Emilie Elvira-Matelot: Institut Jean-Pierre Bourgin for Plant Sciences (IJPB)
Ivan Le Masson: Institut Jean-Pierre Bourgin for Plant Sciences (IJPB)
Aurélie Christ: IPS2
Nathalie Bouteiller: Institut Jean-Pierre Bourgin for Plant Sciences (IJPB)
Martin D. Crespi: IPS2
Hervé Vaucheret: Institut Jean-Pierre Bourgin for Plant Sciences (IJPB)

Nature Communications, 2025, vol. 16, issue 1, 1-14

Abstract: Abstract In plants, aberrant RNAs produced by endogenous genes or transgenes are normally degraded by the nuclear and cytosolic RNA quality control (RQC) pathways. Under certain biotic or abiotic stresses, RQC is impaired, and aberrant RNAs are converted into siRNAs that initiate post-transcriptional gene silencing (PTGS) in the cytosol. How aberrant RNAs are selected and brought to the cytoplasm is not known. Here we show that the RNA-binding protein SUPPRESSOR OF GENE SILENCING (SGS)3 shuttles between the cytosol and the nucleus where it associates with the ISWI-like CHROMATIN REMODELER (CHR)11 and with RNAs transcribed from PTGS-sensitive transgene loci binding CHR11. Knocking down CHR11 and its paralog CHR17 strongly reduces transgene PTGS, suggesting that SGS3 recruitment by CHR11/17 facilitates PTGS initiation. CHR11 is also enriched at endogenous protein-coding genes (PCGs) producing nat-siRNAs and va-siRNAs under biotic or abiotic stresses, and this production is reduced in chr11 chr17 double mutants at genome-wide level. Moreover, impairing CHR11 and CHR17 rescues the lethal phenotype caused by the massive production of siRNAs from PCGs in RQC-deficient mutants. We propose that SGS3 recruitment by CHR11/17 allows exporting RNAs to the cytosol to initiate the production of siRNAs.

Date: 2025
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DOI: 10.1038/s41467-025-57394-5

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