Short-Term Exposure to Nitrogen Dioxide Provides Basal Pathogen Resistance

Plant Physiol. 2018 Sep;178(1):468-487. doi: 10.1104/pp.18.00704. Epub 2018 Aug 3.

Abstract

Nitrogen dioxide (NO2) forms in plants under stress conditions, but little is known about its physiological functions. Here, we explored the physiological functions of NO2 in plant cells using short-term fumigation of Arabidopsis (Arabidopsis thaliana) for 1 h with 10 µL L-1 NO2. Although leaf symptoms were absent, the expression of genes related to pathogen resistance was induced. Fumigated plants developed basal disease resistance, or pattern-triggered immunity, against the necrotrophic fungus Botrytis cinerea and the hemibiotrophic bacterium Pseudomonas syringae Functional salicylic acid and jasmonic acid (JA) signaling pathways were both required for the full expression of NO2-induced resistance against B. cinerea An early peak of salicylic acid accumulation immediately after NO2 exposure was followed by a transient accumulation of oxophytodienoic acid. The simultaneous NO2-induced expression of genes involved in jasmonate biosynthesis and jasmonate catabolism resulted in the complete suppression of JA and JA-isoleucine (JA-Ile) accumulation, which was accompanied by a rise in the levels of their catabolic intermediates 12-OH-JA, 12-OH-JA-Ile, and 12-COOH-JA-Ile. NO2-treated plants emitted the volatile monoterpene α-pinene and the sesquiterpene longifolene (syn. junipene), which could function in signaling or direct defense against pathogens. NO2-triggered B. cinerea resistance was dependent on enhanced early callose deposition and CYTOCHROME P450 79B2 (CYP79B2), CYP79B3, and PHYTOALEXIN DEFICIENT3 gene functions but independent of camalexin, CYP81F2, and 4-OH-indol-3-ylmethylglucosinolate derivatives. In sum, exogenous NO2 triggers basal pathogen resistance, pointing to a possible role for endogenous NO2 in defense signaling. Additionally, this study revealed the involvement of jasmonate catabolism and volatiles in pathogen immunity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics*
  • Arabidopsis / metabolism
  • Arabidopsis / microbiology
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Botrytis / physiology
  • Cyclopentanes / metabolism
  • Cytochrome P-450 Enzyme System / genetics
  • Cytochrome P-450 Enzyme System / metabolism
  • Disease Resistance / drug effects*
  • Disease Resistance / genetics*
  • Gene Expression Regulation, Plant / drug effects
  • Host-Pathogen Interactions / drug effects
  • Nitrogen Dioxide / pharmacology*
  • Oxidants, Photochemical / pharmacology
  • Oxylipins / metabolism
  • Plant Diseases / genetics*
  • Plant Diseases / microbiology
  • Plant Leaves / genetics
  • Plant Leaves / metabolism
  • Plant Leaves / microbiology
  • Pseudomonas syringae / physiology
  • Salicylic Acid / metabolism
  • Time Factors

Substances

  • Arabidopsis Proteins
  • Cyclopentanes
  • Oxidants, Photochemical
  • Oxylipins
  • jasmonic acid
  • Cytochrome P-450 Enzyme System
  • Salicylic Acid
  • Nitrogen Dioxide