S-nitrosylation analysis in Brassica juncea apoplast highlights the importance of nitric oxide in cold-stress signaling

J Proteome Res. 2014 May 2;13(5):2599-619. doi: 10.1021/pr500082u. Epub 2014 Apr 1.

Abstract

Reactive nitrogen species (RNS) including nitric oxide (NO) are important components of stress signaling. However, RNS-mediated signaling in the apoplast remains largely unknown. NO production measured in the shoot apoplast of Brassica juncea seedlings showed nonenzymatic nitrite reduction to NO. Thiol pool quantification showed cold-induced increase in the protein (including S-nitrosothiols) as well as non protein thiols. Proteins from the apoplast were resolved as 109 spots on the 2-D gel, while S-nitrosoglutathione-treated (a NO donor), neutravidin-agarose affinity chromatography-purified S-nitrosylated proteins were resolved as 52 spots. Functional categorization after MALDI-TOF/TOF identification showed 41 and 38% targets to be metabolic/cell-wall-modifying and stress-related, respectively, suggesting the potential role(s) of S-nitrosylation in regulating these responses. Additionally, identification of cold-stress-modulated putative S-nitrosylated proteins by nLC-MS/MS showed that only 38.4% targets with increased S-nitrosylation were secreted by classical pathway, while the majority (61.6%) of these were secreted by unknown/nonclassical pathways. Cold-stress-increased dehydroascorbate reductase and glutathione S-transferase activity via S-nitrosylation and promoted ROS detoxification by ascorbate regeneration and hydrogen peroxide detoxification. Taken together, cold-mediated NO production, thiol pool enrichment, and identification of the 48 putative S-nitrosylated proteins, including 25 novel targets, provided the preview of RNS-mediated cold-stress signaling in the apoplast.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Wall / metabolism
  • Chromatography, Liquid
  • Cold Temperature*
  • Electrophoresis, Gel, Two-Dimensional
  • Extracellular Space / metabolism
  • Models, Biological
  • Mustard Plant / drug effects
  • Mustard Plant / metabolism*
  • Nitric Oxide / metabolism*
  • Nitric Oxide Donors / metabolism
  • Nitric Oxide Donors / pharmacology
  • Plant Proteins / metabolism
  • Proteome / metabolism
  • Proteomics / methods
  • S-Nitrosoglutathione / metabolism
  • S-Nitrosoglutathione / pharmacology
  • S-Nitrosothiols / metabolism
  • Seedlings / drug effects
  • Seedlings / metabolism
  • Signal Transduction / physiology*
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
  • Stress, Physiological / physiology*
  • Sulfhydryl Compounds / metabolism
  • Tandem Mass Spectrometry

Substances

  • Nitric Oxide Donors
  • Plant Proteins
  • Proteome
  • S-Nitrosothiols
  • Sulfhydryl Compounds
  • Nitric Oxide
  • S-Nitrosoglutathione