YUCCA2 (YUC2)-Mediated 3-Indoleacetic Acid (IAA) Biosynthesis Regulates Chloroplast RNA Editing by Relieving the Auxin Response Factor 1 (ARF1)-Dependent Inhibition of Editing Factors in Arabidopsis thaliana

Int J Mol Sci. 2023 Nov 30;24(23):16988. doi: 10.3390/ijms242316988.

Abstract

Although recent research progress on the abundant C-to-U RNA editing events in plant chloroplasts and mitochondria has uncovered many recognition factors and their molecular mechanisms, the intrinsic regulation of RNA editing within plants remains largely unknown. This study aimed to establish a regulatory relationship in Arabidopsis between the plant hormone auxin and chloroplast RNA editing. We first analyzed auxin response elements (AuxREs) present within promoters of chloroplast editing factors reported to date. We found that each has more than one AuxRE, suggesting a potential regulatory role of auxin in their expression. Further investigation unveiled that the depletion of auxin synthesis gene YUC2 reduces the expression of several editing factors. However, in yuc2 mutants, only the expression of CRR4, DYW1, ISE2, and ECD1 editing factors and the editing efficiency of their corresponding editing sites, ndhD-2 and rps14-149, were simultaneously suppressed. In addition, exogenous IAA and the overexpression of YUC2 enhanced the expression of these editing factors and the editing efficiency at the ndhD-2 and rps14-149 sites. These results suggested a direct effect of auxin upon the editing of the ndhD-2 and rps14-149 sites through the modulation of the expression of the editing factors. We further demonstrated that ARF1, a downstream transcription factor in the auxin-signaling pathway, could directly bind to and inactivate the promoters of CRR4, DYW1, and ISE2 in a dual-luciferase reporter system, thereby inhibiting their expression. Moreover, the overexpression of ARF1 in Arabidopsis significantly reduced the expression of the three editing factors and the editing efficiency at the ndhD-2 and rps14-149 sites. These data suggest that YUC2-mediated auxin biosynthesis governs the RNA-editing process through the ARF1-dependent signal transduction pathway.

Keywords: ARF1; RNA editing; YUC2; auxin; chloroplast.

MeSH terms

  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / genetics
  • Arabidopsis* / metabolism
  • Carrier Proteins / metabolism
  • Chloroplasts / genetics
  • Chloroplasts / metabolism
  • DNA-Binding Proteins / metabolism
  • Gene Expression Regulation, Plant
  • Indoleacetic Acids / metabolism
  • RNA Editing
  • RNA, Chloroplast / metabolism
  • Ribosomal Proteins / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Arabidopsis Proteins
  • ARF1 protein, Arabidopsis
  • Carrier Proteins
  • DNA-Binding Proteins
  • DYW1 protein, Arabidopsis
  • indoleacetic acid
  • Indoleacetic Acids
  • Ribosomal Proteins
  • RNA, Chloroplast
  • Transcription Factors
  • YUCCA2 protein, Arabidopsis