Role of tomato lipoxygenase D in wound-induced jasmonate biosynthesis and plant immunity to insect herbivores

PLoS Genet. 2013;9(12):e1003964. doi: 10.1371/journal.pgen.1003964. Epub 2013 Dec 12.

Abstract

In response to insect attack and mechanical wounding, plants activate the expression of genes involved in various defense-related processes. A fascinating feature of these inducible defenses is their occurrence both locally at the wounding site and systemically in undamaged leaves throughout the plant. Wound-inducible proteinase inhibitors (PIs) in tomato (Solanum lycopersicum) provide an attractive model to understand the signal transduction events leading from localized injury to the systemic expression of defense-related genes. Among the identified intercellular molecules in regulating systemic wound response of tomato are the peptide signal systemin and the oxylipin signal jasmonic acid (JA). The systemin/JA signaling pathway provides a unique opportunity to investigate, in a single experimental system, the mechanism by which peptide and oxylipin signals interact to coordinate plant systemic immunity. Here we describe the characterization of the tomato suppressor of prosystemin-mediated responses8 (spr8) mutant, which was isolated as a suppressor of (pro)systemin-mediated signaling. spr8 plants exhibit a series of JA-dependent immune deficiencies, including the inability to express wound-responsive genes, abnormal development of glandular trichomes, and severely compromised resistance to cotton bollworm (Helicoverpa armigera) and Botrytis cinerea. Map-based cloning studies demonstrate that the spr8 mutant phenotype results from a point mutation in the catalytic domain of TomLoxD, a chloroplast-localized lipoxygenase involved in JA biosynthesis. We present evidence that overexpression of TomLoxD leads to elevated wound-induced JA biosynthesis, increased expression of wound-responsive genes and, therefore, enhanced resistance to insect herbivory attack and necrotrophic pathogen infection. These results indicate that TomLoxD is involved in wound-induced JA biosynthesis and highlight the application potential of this gene for crop protection against insects and pathogens.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Botrytis / pathogenicity
  • Chloroplast Proteins / genetics*
  • Chloroplasts / enzymology
  • Cyclopentanes / metabolism*
  • Gene Expression Regulation, Plant
  • Herbivory
  • Lipoxygenase / genetics*
  • Lipoxygenases / genetics*
  • Lipoxygenases / immunology
  • Molecular Sequence Data
  • Oxylipins / metabolism*
  • Phenotype
  • Plant Diseases / genetics
  • Plant Immunity*
  • Plant Proteins / antagonists & inhibitors
  • Plant Proteins / genetics
  • Signal Transduction
  • Solanum lycopersicum / enzymology*
  • Wounds and Injuries

Substances

  • Chloroplast Proteins
  • Cyclopentanes
  • Oxylipins
  • Plant Proteins
  • prosystemin protein, Lycopersicon esculentum
  • jasmonic acid
  • Lipoxygenases
  • Lipoxygenase

Associated data

  • GENBANK/AAB65766
  • GENBANK/AAB65767
  • GENBANK/AAB67865
  • GENBANK/AAD09202
  • GENBANK/AAG21691
  • GENBANK/ACL81190
  • GENBANK/CAA58859
  • GENBANK/CAA65268
  • GENBANK/CAA65269
  • GENBANK/CAC12843
  • GENBANK/O24370
  • GENBANK/O24371
  • RefSeq/NP_001049158
  • RefSeq/NP_001099263
  • RefSeq/NP_001234259
  • RefSeq/NP_033792
  • RefSeq/XP_003528556
  • SWISSPROT/P38415
  • SWISSPROT/P38416

Grants and funding

This work was supported by the Ministry of Agriculture of China (2013ZX08009-003-001), the Ministry of Science and Technology of China (2012CB114105, 2013AA102603, 2012CB113902, 2012AA100101), the Beijing Natural Science Foundation (6120001), and the National Natural Science Foundation of China (31030006). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.