Ethylene-independent modulation of root development by ACC via downregulation of WOX5 and group I CLE peptide expression

Proc Natl Acad Sci U S A. 2025 Feb 11;122(6):e2417735122. doi: 10.1073/pnas.2417735122. Epub 2025 Feb 5.

Abstract

In seed plants, the canonical role of 1-aminocyclopropane-1-carboxylic acid (ACC) is to serve as the precursor in the biosynthesis of the phytohormone ethylene, and indeed, ACC treatment is often used as a proxy for ethylene treatment. Increasing evidence suggests that ACC can also act independently of ethylene to regulate various aspects of plant growth and development. Here, we explore the effects of ACC on Arabidopsis thaliana root growth and the mechanisms by which it acts. ACC inhibits growth of the primary root in Arabidopsis seedlings when ethylene signaling is blocked, which becomes evident after 36 h of treatment with ACC. This reduced root growth is in part the result of suppressed cell proliferation in the root meristem resulting from altered expression of a key regulator of stem cell niche activity, WOX5. ACC also promotes lateral root (LR) development, in contrast to ethylene, which inhibits LR formation. Transcriptomic analysis of roots revealed no significant changes in gene expression after 45 min or 4 h of ACC treatment, but longer treatment times revealed a large number of differentially expressed genes, including the downregulation of the expression of a small group of phylogenetically related CLE peptides. Reduced expression of these group 1 CLEs in response to ACC leads to the activation of a transcription factor, LBD18, which promotes LR development. These results suggest that ACC acts to modulate multiple aspects of Arabidopsis root growth independently of ethylene via distinct transcriptional effects in the root meristem and LR precursor cells.

Keywords: ACC; CLE peptides; ethylene; lateral roots; root development.

MeSH terms

  • Amino Acids, Cyclic* / metabolism
  • Amino Acids, Cyclic* / pharmacology
  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / drug effects
  • Arabidopsis* / genetics
  • Arabidopsis* / growth & development
  • Arabidopsis* / metabolism
  • Down-Regulation / drug effects
  • Ethylenes* / metabolism
  • Gene Expression Regulation, Plant* / drug effects
  • Homeodomain Proteins* / genetics
  • Homeodomain Proteins* / metabolism
  • Meristem / drug effects
  • Meristem / growth & development
  • Meristem / metabolism
  • Plant Roots* / drug effects
  • Plant Roots* / genetics
  • Plant Roots* / growth & development
  • Plant Roots* / metabolism
  • Signal Transduction

Substances

  • Ethylenes
  • Arabidopsis Proteins
  • ethylene
  • Amino Acids, Cyclic
  • 1-aminocyclopropane-1-carboxylic acid
  • Homeodomain Proteins
  • WUSCHEL protein, Arabidopsis
  • AT2G27250 protein, Arabidopsis