Bacterial type III effector-induced plant C8 volatiles elicit antibacterial immunity in heterospecific neighbouring plants via airborne signalling

Plant Cell Environ. 2022 Jan;45(1):236-247. doi: 10.1111/pce.14209. Epub 2021 Nov 6.

Abstract

Upon sensing attack by pathogens and insect herbivores, plants release complex mixtures of volatile compounds. Here, we show that the infection of lima bean (Phaseolus lunatus L.) plants with the non-host bacterial pathogen Pseudomonas syringae pv. tomato led to the production of microbe-induced plant volatiles (MIPVs). Surprisingly, the bacterial type III secretion system, which injects effector proteins directly into the plant cytosol to subvert host functions, was found to prime both intra- and inter-specific defense responses in neighbouring wild tobacco (Nicotiana benthamiana) plants. Screening of each of 16 effectors using the Pseudomonas fluorescens effector-to-host analyser revealed that an effector, HopP1, was responsible for immune activation in receiver tobacco plants. Further study demonstrated that 1-octen-3-ol, 3-octanone and 3-octanol are novel MIPVs emitted by the lima bean plant in a HopP1-dependent manner. Exposure to synthetic 1-octen-3-ol activated immunity in tobacco plants against a virulent pathogen Pseudomonas syringae pv. tabaci. Our results show for the first time that a bacterial type III effector can trigger the emission of C8 plant volatiles that mediate defense priming via plant-plant interactions. These results provide novel insights into the role of airborne chemicals in bacterial pathogen-induced inter-specific plant-plant interactions.

Keywords: 1-octen-3-ol; C8 volatiles; airborne defense; lima bean; plant-plant interactions; self- and non-self-recognition; tobacco; type III effector.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Air
  • Capsicum / physiology
  • Cucumis sativus / physiology
  • Gene Expression Regulation, Plant
  • Host-Pathogen Interactions / physiology*
  • Nicotiana / physiology
  • Octanols / pharmacology
  • Phaseolus / physiology
  • Plant Immunity* / drug effects
  • Pseudomonas syringae / pathogenicity*
  • Signal Transduction
  • Type III Secretion Systems / physiology*
  • Volatile Organic Compounds / metabolism*
  • Volatile Organic Compounds / pharmacology

Substances

  • Octanols
  • Type III Secretion Systems
  • Volatile Organic Compounds
  • 1-octen-3-ol