Reactive oxygen species and reactive carbonyl species constitute a feed-forward loop in auxin signaling for lateral root formation

Plant J. 2019 Nov;100(3):536-548. doi: 10.1111/tpj.14456. Epub 2019 Aug 21.

Abstract

In auxin-stimulated roots, production of reactive oxygen species (ROS) via the hormone-induced activation of respiratory burst oxidase homologous NADPH oxidases facilitates lateral root (LR) formation. In this study, in order to verify that ROS can modulate auxin signaling, we examined the involvement of the lipid peroxide-derived agents known as reactive carbonyl species (RCS) in LR formation. When auxin was added to Arabidopsis thaliana roots, the levels of RCS, for example acrolein, 4-hydroxynonenal and crotonaldehyde, were increased prior to LR formation. Addition of the carbonyl scavenger carnosine suppressed auxin-induced LR formation. Addition of RCS to the roots induced the expression of the auxin-responsive DR5 promoter and the TIR1, IAA14, ARF7, LBD16 and PUCHI genes and facilitated LR formation without increasing the endogenous auxin level. DR5 and LBD16 were activated in the LR primordia. The auxin signaling-deficient mutants arf7 arf19 and slr-1 did not respond - and tir1 afb2 appeared to show a poor response - to RCS. When given to the roots RCS promoted the disappearance of the AXR3NT-GUS fusion protein, i.e. the degradation of the auxin/indole-3-acetic acid protein, as did auxin. These results indicate that the auxin-induced production of ROS and their downstream products RCS modulate the auxin signaling pathway in a feed-forward manner. RCS are key agents that connect the ROS signaling and the auxin signaling pathways.

Keywords: Arabidopsis thaliana; hormonal signal; oxylipin; reactive carbonyl species; reactive electrophile species; reactive oxygen species.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / growth & development
  • Arabidopsis / physiology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Free Radicals / metabolism*
  • Genes, Reporter
  • Indoleacetic Acids / metabolism*
  • Lipid Peroxides / metabolism
  • Oxylipins / metabolism
  • Plant Growth Regulators / metabolism*
  • Plant Roots / genetics
  • Plant Roots / growth & development
  • Plant Roots / physiology
  • Promoter Regions, Genetic / genetics
  • Reactive Oxygen Species / metabolism*
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Signal Transduction*

Substances

  • Arabidopsis Proteins
  • Free Radicals
  • Indoleacetic Acids
  • Lipid Peroxides
  • Oxylipins
  • Plant Growth Regulators
  • Reactive Oxygen Species
  • Repressor Proteins
  • indoleacetic acid