Evidence for the Involvement of Auxin, Ethylene and ROS Signaling During Primary Root Inhibition of Arabidopsis by the Allelochemical Benzoic Acid

Plant Cell Physiol. 2018 Sep 1;59(9):1889-1904. doi: 10.1093/pcp/pcy107.

Abstract

Allelopathy is mediated by plant-derived secondary metabolites (allelochemicals) which are released by donor plants and affect the growth and development of receptor plants. The plant root is the first organ which senses soil allelochemicals this results in the production of a shorter primary root. However, the mechanisms underlying this process remain elusive. Here, we report that a model allelochemical benzoic acid (BA) inhibited primary root elongation of Arabidopsis seedlings by reducing the sizes of both the meristem and elongation zones, and that auxin signaling affected this process. An increase in auxin level in the root tips was associated with increased expression of auxin biosynthesis genes and auxin polar transporter AUX1 and PIN2 genes under BA stress. Mutant analyses demonstrated that AUX1 and PIN2 rather than PIN1 were required for the inhibition of primary root elongation during BA exposure. Furthermore, BA stimulated ethylene evolution, whereas blocking BA-induced ethylene signaling with an ethylene biosynthesis inhibitor (Co2+), an ethylene perception antagonist (1-methylcyclopropene) or ethylene signaling mutant lines etr1-3 and ein3eil1 compromised BA-mediated inhibition of root elongation and up-regulation of auxin biosynthesis-related genes together with AUX1 and PIN2, indicating that ethylene signal was involved in auxin-mediated inhibition of primary root elongation during BA stress. Further analysis revealed that the BA-induced reactive oxygen species (ROS) burst contributed to BA-mediated root growth inhibition without affecting auxin and ethylene signals. Taken together, our results reveal that the allelochemical BA inhibits root elongation by increasing auxin accumulation via stimulation of auxin biosynthesis and AUX1/PIN2-mediated auxin transport via stimulation of ethylene production and an auxin/ethylene-independent ROS burst.

Keywords: Arabidopsis thaliana; Allelopathy; Auxin transport; Benzoic acid; Ethylene; Reactive oxygen species.

MeSH terms

  • Arabidopsis / physiology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Benzoic Acid / pharmacology*
  • Ethylenes / metabolism*
  • Gene Expression Regulation, Plant / drug effects
  • Indoleacetic Acids / metabolism*
  • Plant Roots / drug effects*
  • Plant Roots / growth & development
  • Reactive Oxygen Species / metabolism*
  • Signal Transduction

Substances

  • Arabidopsis Proteins
  • Ethylenes
  • Indoleacetic Acids
  • Reactive Oxygen Species
  • Benzoic Acid
  • ethylene