High levels of cyclic-di-GMP in plant-associated Pseudomonas correlate with evasion of plant immunity

Mol Plant Pathol. 2016 May;17(4):521-31. doi: 10.1111/mpp.12297. Epub 2015 Oct 8.

Abstract

The plant innate immune system employs plasma membrane-localized receptors that specifically perceive pathogen/microbe-associated molecular patterns (PAMPs/MAMPs). This induces a defence response called pattern-triggered immunity (PTI) to fend off pathogen attack. Commensal bacteria are also exposed to potential immune recognition and must employ strategies to evade and/or suppress PTI to successfully colonize the plant. During plant infection, the flagellum has an ambiguous role, acting as both a virulence factor and also as a potent immunogen as a result of the recognition of its main building block, flagellin, by the plant pattern recognition receptors (PRRs), including FLAGELLIN SENSING2 (FLS2). Therefore, strict control of flagella synthesis is especially important for plant-associated bacteria. Here, we show that cyclic-di-GMP [bis-(3'-5')-cyclic di-guanosine monophosphate], a central regulator of bacterial lifestyle, is involved in the evasion of PTI. Elevated cyclic-di-GMP levels in the pathogen Pseudomonas syringae pv. tomato (Pto) DC3000, the opportunist P. aeruginosa PAO1 and the commensal P. protegens Pf-5 inhibit flagellin synthesis and help the bacteria to evade FLS2-mediated signalling in Nicotiana benthamiana and Arabidopsis thaliana. Despite this, high cellular cyclic-di-GMP concentrations were shown to drastically reduce the virulence of Pto DC3000 during plant infection. We propose that this is a result of reduced flagellar motility and/or additional pleiotropic effects of cyclic-di-GMP signalling on bacterial behaviour.

Keywords: PTI; Pseudomonas; cyclic-di-GMP; flagellin; immune evasion.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / immunology
  • Arabidopsis / microbiology*
  • Cyclic GMP / analogs & derivatives*
  • Cyclic GMP / metabolism
  • Flagellin / pharmacology
  • Gene Expression Regulation, Bacterial / drug effects
  • Immune Evasion* / drug effects
  • Nicotiana / immunology
  • Nicotiana / microbiology*
  • Plant Diseases / genetics
  • Plant Diseases / immunology
  • Plant Diseases / microbiology
  • Plant Immunity* / drug effects
  • Pseudomonas syringae / drug effects
  • Pseudomonas syringae / genetics
  • Pseudomonas syringae / immunology*
  • Pseudomonas syringae / pathogenicity
  • Reactive Oxygen Species / metabolism
  • Virulence / drug effects
  • Virulence / genetics

Substances

  • Reactive Oxygen Species
  • Flagellin
  • bis(3',5')-cyclic diguanylic acid
  • Cyclic GMP