Role of Tomato Lipoxygenase D in Wound-Induced Jasmonate Biosynthesis and Plant Immunity to Insect Herbivores
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 pla...
Autores principales: | , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2013
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3861047/ https://www.ncbi.nlm.nih.gov/pubmed/24348260 http://dx.doi.org/10.1371/journal.pgen.1003964 |
_version_ | 1782295591219363840 |
---|---|
author | Yan, Liuhua Zhai, Qingzhe Wei, Jianing Li, Shuyu Wang, Bao Huang, Tingting Du, Minmin Sun, Jiaqiang Kang, Le Li, Chang-Bao Li, Chuanyou |
author_facet | Yan, Liuhua Zhai, Qingzhe Wei, Jianing Li, Shuyu Wang, Bao Huang, Tingting Du, Minmin Sun, Jiaqiang Kang, Le Li, Chang-Bao Li, Chuanyou |
author_sort | Yan, Liuhua |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-3861047 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2013 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-38610472013-12-17 Role of Tomato Lipoxygenase D in Wound-Induced Jasmonate Biosynthesis and Plant Immunity to Insect Herbivores Yan, Liuhua Zhai, Qingzhe Wei, Jianing Li, Shuyu Wang, Bao Huang, Tingting Du, Minmin Sun, Jiaqiang Kang, Le Li, Chang-Bao Li, Chuanyou PLoS Genet Research Article 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. Public Library of Science 2013-12-12 /pmc/articles/PMC3861047/ /pubmed/24348260 http://dx.doi.org/10.1371/journal.pgen.1003964 Text en © 2013 Yan et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. |
spellingShingle | Research Article Yan, Liuhua Zhai, Qingzhe Wei, Jianing Li, Shuyu Wang, Bao Huang, Tingting Du, Minmin Sun, Jiaqiang Kang, Le Li, Chang-Bao Li, Chuanyou Role of Tomato Lipoxygenase D in Wound-Induced Jasmonate Biosynthesis and Plant Immunity to Insect Herbivores |
title | Role of Tomato Lipoxygenase D in Wound-Induced Jasmonate Biosynthesis and Plant Immunity to Insect Herbivores |
title_full | Role of Tomato Lipoxygenase D in Wound-Induced Jasmonate Biosynthesis and Plant Immunity to Insect Herbivores |
title_fullStr | Role of Tomato Lipoxygenase D in Wound-Induced Jasmonate Biosynthesis and Plant Immunity to Insect Herbivores |
title_full_unstemmed | Role of Tomato Lipoxygenase D in Wound-Induced Jasmonate Biosynthesis and Plant Immunity to Insect Herbivores |
title_short | Role of Tomato Lipoxygenase D in Wound-Induced Jasmonate Biosynthesis and Plant Immunity to Insect Herbivores |
title_sort | role of tomato lipoxygenase d in wound-induced jasmonate biosynthesis and plant immunity to insect herbivores |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3861047/ https://www.ncbi.nlm.nih.gov/pubmed/24348260 http://dx.doi.org/10.1371/journal.pgen.1003964 |
work_keys_str_mv | AT yanliuhua roleoftomatolipoxygenasedinwoundinducedjasmonatebiosynthesisandplantimmunitytoinsectherbivores AT zhaiqingzhe roleoftomatolipoxygenasedinwoundinducedjasmonatebiosynthesisandplantimmunitytoinsectherbivores AT weijianing roleoftomatolipoxygenasedinwoundinducedjasmonatebiosynthesisandplantimmunitytoinsectherbivores AT lishuyu roleoftomatolipoxygenasedinwoundinducedjasmonatebiosynthesisandplantimmunitytoinsectherbivores AT wangbao roleoftomatolipoxygenasedinwoundinducedjasmonatebiosynthesisandplantimmunitytoinsectherbivores AT huangtingting roleoftomatolipoxygenasedinwoundinducedjasmonatebiosynthesisandplantimmunitytoinsectherbivores AT duminmin roleoftomatolipoxygenasedinwoundinducedjasmonatebiosynthesisandplantimmunitytoinsectherbivores AT sunjiaqiang roleoftomatolipoxygenasedinwoundinducedjasmonatebiosynthesisandplantimmunitytoinsectherbivores AT kangle roleoftomatolipoxygenasedinwoundinducedjasmonatebiosynthesisandplantimmunitytoinsectherbivores AT lichangbao roleoftomatolipoxygenasedinwoundinducedjasmonatebiosynthesisandplantimmunitytoinsectherbivores AT lichuanyou roleoftomatolipoxygenasedinwoundinducedjasmonatebiosynthesisandplantimmunitytoinsectherbivores |