The chloroplast-localized phospholipases D α4 and α5 regulate herbivore-induced direct and indirect defenses in rice

Plant Physiol. 2011 Dec;157(4):1987-99. doi: 10.1104/pp.111.183749. Epub 2011 Oct 7.

Abstract

The oxylipin pathway is of central importance for plant defensive responses. Yet, the first step of the pathway, the liberation of linolenic acid following induction, is poorly understood. Phospholipases D (PLDs) have been hypothesized to mediate this process, but data from Arabidopsis (Arabidopsis thaliana) regarding the role of PLDs in plant resistance have remained controversial. Here, we cloned two chloroplast-localized PLD genes from rice (Oryza sativa), OsPLDα4 and OsPLDα5, both of which were up-regulated in response to feeding by the rice striped stem borer (SSB) Chilo suppressalis, mechanical wounding, and treatment with jasmonic acid (JA). Antisense expression of OsPLDα4 and -α5 (as-pld), which resulted in a 50% reduction of the expression of the two genes, reduced elicited levels of linolenic acid, JA, green leaf volatiles, and ethylene and attenuated the SSB-induced expression of a mitogen-activated protein kinase (OsMPK3), a lipoxygenase (OsHI-LOX), a hydroperoxide lyase (OsHPL3), as well as a 1-aminocyclopropane-1-carboxylic acid synthase (OsACS2). The impaired oxylipin and ethylene signaling in as-pld plants decreased the levels of herbivore-induced trypsin protease inhibitors and volatiles, improved the performance of SSB and the rice brown planthopper Nilaparvata lugens, and reduced the attractiveness of plants to a larval parasitoid of SSB, Apanteles chilonis. The production of trypsin protease inhibitors in as-pld plants could be partially restored by JA, while the resistance to rice brown planthopper and SSB was restored by green leaf volatile application. Our results show that phospholipases function as important components of herbivore-induced direct and indirect defenses in rice.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Chloroplast Proteins / genetics
  • Chloroplast Proteins / metabolism
  • Chloroplasts / enzymology*
  • Chloroplasts / metabolism
  • Cyclopentanes / pharmacology
  • Disease Resistance
  • Ethylenes / analysis
  • Ethylenes / metabolism
  • Gene Expression Regulation, Plant
  • Hemiptera / physiology
  • Herbivory
  • Lepidoptera / physiology
  • Oils, Volatile / analysis
  • Oils, Volatile / metabolism
  • Oryza / enzymology*
  • Oryza / genetics
  • Oryza / immunology*
  • Oryza / metabolism
  • Oxylipins / analysis
  • Oxylipins / metabolism
  • Oxylipins / pharmacology
  • Phospholipase D / genetics
  • Phospholipase D / metabolism*
  • Plant Diseases / immunology*
  • Plant Diseases / parasitology
  • Plant Oils / analysis
  • Plant Oils / metabolism
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Plants, Genetically Modified
  • RNA, Antisense
  • Signal Transduction
  • alpha-Linolenic Acid / analysis
  • alpha-Linolenic Acid / metabolism

Substances

  • Chloroplast Proteins
  • Cyclopentanes
  • Ethylenes
  • Oils, Volatile
  • Oxylipins
  • Plant Oils
  • Plant Proteins
  • RNA, Antisense
  • alpha-Linolenic Acid
  • jasmonic acid
  • ethylene
  • Phospholipase D