Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism

Proc Natl Acad Sci U S A. 2013 Sep 3;110(36):14807-12. doi: 10.1073/pnas.1302702110. Epub 2013 Aug 19.

Abstract

The plant hormone salicylic acid (SA) plays critical roles in plant defense, stress responses, and senescence. Although SA biosynthesis is well understood, the pathways by which SA is catabolized remain elusive. Here we report the identification and characterization of an SA 3-hydroxylase (S3H) involved in SA catabolism during leaf senescence. S3H is associated with senescence and is inducible by SA and is thus a key part of a negative feedback regulation system of SA levels during senescence. The enzyme converts SA (with a Km of 58.29 µM) to both 2,3-dihydroxybenzoic acid (2,3-DHBA) and 2,5-DHBA in vitro but only 2,3-DHBA in vivo. The s3h knockout mutants fail to produce 2,3-DHBA sugar conjugates, accumulate very high levels of SA and its sugar conjugates, and exhibit a precocious senescence phenotype. Conversely, the gain-of-function lines contain high levels of 2,3-DHBA sugar conjugates and extremely low levels of SA and its sugar conjugates and display a significantly extended leaf longevity. This research reveals an elegant SA catabolic mechanism by which plants regulate SA levels by converting it to 2,3-DHBA to prevent SA overaccumulation. The research also provides strong molecular genetic evidence for an important role of SA in regulating the onset and rate of leaf senescence.

Keywords: NahG; aging; benzoic acid; disease resistance; senescence-associated gene.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Arabidopsis / genetics*
  • Arabidopsis / physiology
  • Arabidopsis Proteins / classification
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism
  • Biocatalysis
  • Gene Expression Regulation, Enzymologic / drug effects
  • Gene Expression Regulation, Plant / drug effects
  • Gentisates / chemistry
  • Gentisates / metabolism
  • Hydroxybenzoates / chemistry
  • Hydroxybenzoates / metabolism
  • Kinetics
  • Mass Spectrometry
  • Mixed Function Oxygenases / classification
  • Mixed Function Oxygenases / genetics*
  • Mixed Function Oxygenases / metabolism
  • Molecular Sequence Data
  • Molecular Structure
  • Mutation
  • Phylogeny
  • Plant Leaves / chemistry
  • Plant Leaves / genetics*
  • Plant Leaves / physiology
  • Plants, Genetically Modified
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Salicylic Acid / metabolism*
  • Salicylic Acid / pharmacology
  • Sequence Homology, Amino Acid

Substances

  • Arabidopsis Proteins
  • Gentisates
  • Hydroxybenzoates
  • RNA, Messenger
  • 2,3-dihydroxybenzoic acid
  • Mixed Function Oxygenases
  • salicylic acid 3-hydroxylase, Arabidopsis
  • Salicylic Acid
  • 2,5-dihydroxybenzoic acid