Jasmonate-dependent modifications of the pectin matrix during potato development function as a defense mechanism targeted by Dickeya dadantii virulence factors

Plant J. 2014 Feb;77(3):418-29. doi: 10.1111/tpj.12393. Epub 2014 Jan 16.

Abstract

The plant cell wall constitutes an essential protection barrier against pathogen attack. In addition, cell-wall disruption leads to accumulation of jasmonates (JAs), which are key signaling molecules for activation of plant inducible defense responses. However, whether JAs in return modulate the cell-wall composition to reinforce this defensive barrier remains unknown. The enzyme 13-allene oxide synthase (13-AOS) catalyzes the first committed step towards biosynthesis of JAs. In potato (Solanum tuberosum), there are two putative St13-AOS genes, which we show here to be differentially induced upon wounding. We also determine that both genes complement an Arabidopsis aos null mutant, indicating that they encode functional 13-AOS enzymes. Indeed, transgenic potato plants lacking both St13-AOS genes (CoAOS1/2 lines) exhibited a significant reduction of JAs, a concomitant decrease in wound-responsive gene activation, and an increased severity of soft rot disease symptoms caused by Dickeya dadantii. Intriguingly, a hypovirulent D. dadantii pel strain lacking the five major pectate lyases, which causes limited tissue maceration on wild-type plants, regained infectivity in CoAOS1/2 plants. In line with this, we found differences in pectin methyl esterase activity and cell-wall pectin composition between wild-type and CoAOS1/2 plants. Importantly, wild-type plants had pectins with a lower degree of methyl esterification, which are the substrates of the pectate lyases mutated in the pel strain. These results suggest that, during development of potato plants, JAs mediate modification of the pectin matrix to form a defensive barrier that is counteracted by pectinolytic virulence factors from D. dadantii.

Keywords: Dickeya; OPDA; allene oxide synthase; cell wall; jasmonic acid; pectin methyl-esterification.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / enzymology
  • Arabidopsis / genetics
  • Arabidopsis / immunology
  • Arabidopsis / microbiology
  • Bacterial Proteins / metabolism
  • Carboxylic Ester Hydrolases / genetics
  • Carboxylic Ester Hydrolases / metabolism
  • Cell Wall / metabolism
  • Cyclopentanes / metabolism*
  • Disease Resistance
  • Enterobacteriaceae / enzymology
  • Enterobacteriaceae / pathogenicity*
  • Esterification
  • Host-Pathogen Interactions
  • Intramolecular Oxidoreductases / genetics
  • Intramolecular Oxidoreductases / metabolism*
  • Mutation
  • Oxylipins / metabolism*
  • Pectins / metabolism*
  • Plant Diseases / immunology*
  • Plant Diseases / microbiology
  • Plant Growth Regulators / metabolism*
  • Plant Leaves / enzymology
  • Plant Leaves / genetics
  • Plant Leaves / immunology
  • Plant Leaves / microbiology
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Plants, Genetically Modified
  • Polysaccharide-Lyases / genetics
  • Polysaccharide-Lyases / metabolism
  • Solanum tuberosum / enzymology
  • Solanum tuberosum / genetics
  • Solanum tuberosum / immunology*
  • Solanum tuberosum / microbiology
  • Virulence Factors
  • Wounds and Injuries

Substances

  • Bacterial Proteins
  • Cyclopentanes
  • Oxylipins
  • Plant Growth Regulators
  • Plant Proteins
  • Virulence Factors
  • jasmonic acid
  • Pectins
  • Carboxylic Ester Hydrolases
  • pectinesterase
  • Polysaccharide-Lyases
  • pectate lyase
  • Intramolecular Oxidoreductases
  • hydroperoxide isomerase