Lipo-chitooligosaccharide signalling blocks a rapid pathogen-induced ROS burst without impeding immunity

New Phytol. 2019 Jan;221(2):743-749. doi: 10.1111/nph.15574. Epub 2018 Nov 26.

Abstract

Molecular signals released by microbes at the surface of plant roots and leaves largely determine host responses, notably by triggering either immunity or symbiosis. How these signalling pathways cross-talk upon coincident perception of pathogens and symbionts is poorly described in plants forming symbiosis. Nitrogen fixing symbiotic Rhizobia spp. and arbuscular mycorrhizal fungi produce lipo-chitooligosaccharides (LCOs) to initiate host symbiotic programmes. In Medicago truncatula roots, the perception of LCOs leads to reduced efflux of reactive oxygen species (ROS). By contrast, pathogen perception generally triggers a strong ROS burst and activates defence gene expression. Here we show that incubation of M. truncatula seedlings with culture filtrate (CF) of the legume pathogen Aphanomyces euteiches alone or simultaneously with Sinorhizobium meliloti LCOs, resulted in a strong ROS release. However, this response was completely inhibited if CF was added after pre-incubation of seedlings with LCOs. By contrast, expression of immunity-associated genes in response to CF and disease resistance to A. euteiches remained unaffected by LCO treatment of M. truncatula roots. Our findings suggest that symbiotic plants evolved ROS inhibition response to LCOs to facilitate early steps of symbiosis whilst maintaining a parallel defence mechanisms toward pathogens.

Keywords: Aphanomyces euteiches; Medicago truncatula; immunity; lipo-chitooligosaccharide (LOS); oomycete; reactive oxygen species (ROS); symbiosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aphanomyces / physiology*
  • Chitin / analogs & derivatives*
  • Chitin / metabolism
  • Chitosan
  • Disease Resistance
  • Gene Expression Regulation, Plant
  • Lipids / chemistry*
  • Medicago truncatula / genetics
  • Medicago truncatula / immunology*
  • Medicago truncatula / microbiology*
  • Oligosaccharides
  • Plant Diseases / immunology
  • Plant Diseases / microbiology
  • Plant Immunity* / genetics
  • Plant Roots / genetics
  • Plant Roots / microbiology
  • Reactive Oxygen Species / metabolism*
  • Seedlings / growth & development
  • Seedlings / physiology
  • Signal Transduction*
  • Sinorhizobium meliloti / physiology

Substances

  • Lipids
  • Oligosaccharides
  • Reactive Oxygen Species
  • oligochitosan
  • Chitin
  • Chitosan