ALTERED MERISTEM PROGRAM1 impairs RNA silencing by repressing the biogenesis of a subset of inverted repeat-derived siRNAs

Plant Cell. 2024 Dec 23;37(1):koae293. doi: 10.1093/plcell/koae293.

Abstract

RNA silencing negatively regulates gene expression at the transcriptional and posttranscriptional levels through DNA methylation, histone modification, mRNA cleavage, and translational inhibition. Small interfering RNAs (siRNAs) of 21 to 24 nucleotides are processed from double-stranded RNAs by Dicer-like (DCL) enzymes and play essential roles in RNA silencing in plants. Here, we demonstrated that ALTERED MERISTEM PROGRAM1 (AMP1) and its putative paralog LIKE AMP1 (LAMP1) impair RNA silencing by repressing the biogenesis of a subset of inverted repeat (IR)-derived siRNAs in Arabidopsis (Arabidopsis thaliana). AMP1 and LAMP1 inhibit Pol II-dependent IR gene transcription by suppressing ARGONAUTE 1 (AGO1) protein levels. Genetic analysis indicates that AMP1 acts upstream of RNA polymerase IV subunit 1 (NRPD1), RNA-dependent RNA polymerase 2 (RDR2), and DCL4, which are required for IR-induced RNA silencing. We also show that AMP1 and LAMP1 inhibit siRNA-mediated silencing in a different mechanism from that of AGO4 and DCL3. Together, these results reveal two previously unknown players in siRNA biogenesis from IRs-AGO1, which promotes IR transcription, and AMP1, which inhibits IR transcription indirectly through the repression of AGO1 expression.

MeSH terms

  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / genetics
  • Arabidopsis* / metabolism
  • Argonaute Proteins* / genetics
  • Argonaute Proteins* / metabolism
  • DNA-Directed RNA Polymerases
  • Gene Expression Regulation, Plant*
  • Inverted Repeat Sequences / genetics
  • RNA Interference*
  • RNA Polymerase II / genetics
  • RNA Polymerase II / metabolism
  • RNA, Small Interfering* / genetics
  • RNA, Small Interfering* / metabolism
  • RNA-Dependent RNA Polymerase / genetics
  • RNA-Dependent RNA Polymerase / metabolism
  • Ribonuclease III / genetics
  • Ribonuclease III / metabolism

Substances

  • Arabidopsis Proteins
  • RNA, Small Interfering
  • Argonaute Proteins
  • AGO1 protein, Arabidopsis
  • RNA-Dependent RNA Polymerase
  • Ribonuclease III
  • DCL4 protein, Arabidopsis
  • RDR2 protein, Arabidopsis
  • RNA Polymerase II
  • NRPD1A protein, Arabidopsis
  • DNA-Directed RNA Polymerases