Abstract
Hydrogen peroxide (H2O2) generated in response to wounding can be detected at wound sites and in distal leaf veins within 1 hr after wounding. The response is systemic and maximizes at about 4-6 hr in both wounded and unwounded leaves, and then declines. The timing of the response corresponds with an increase in wound-inducible polygalacturonase (PG) mRNA and enzyme activity previously reported, suggesting that oligogalacturonic acid (OGA) fragments produced by PG are triggering the H2O2 response. Systemin, OGA, chitosan, and methyl jasmonate (MJ) all induce the accumulation of H2O2 in leaves. Tomato plants transformed with an antisense prosystemin gene produce neither PG activity or H2O2 in leaves in response to wounding, implicating systemin as a primary wound signal. The antisense plants do produce both PG activity and H2O2 when supplied with systemin, OGA, chitosan, or MJ. A mutant tomato line compromised in the octadecanoid pathway does not exhibit PG activity or H2O2 in response to wounding, systemin, OGA, or chitosan, but does respond to MJ, indicating that the generation of H2O2 requires a functional octadecanoid signaling pathway. Among 18 plant species from six families that were assayed for wound-inducible PG activity and H2O2 generation, 14 species exhibited both wound-inducible PG activity and the generation of H2O2. Four species, all from the Fabaceae family, exhibited little or no wound-inducible PG activity and did not generate H2O2. The time course of wound-inducible PG activity and H2O2 in Arabidopsis thaliana leaves was similar to that found in tomato. The cumulative data suggest that systemic wound signals that induce PG activity and H2O2 are widespread in the plant kingdom and that the response may be associated with the defense of plants against both herbivores and pathogens.
MeSH Terms
Hydrogen Peroxide/metabolism
Oligodeoxyribonucleotides, Antisense/pharmacology
Peptides/genetics,metabolism
Plant Leaves/drug effects,metabolism
Plant Proteins/metabolism
Plants/genetics,metabolism
Plants, Edible/metabolism
Polygalacturonase/genetics,metabolism
Reactive Oxygen Species/metabolism
Species Specificity
Transcription, Genetic
Chemicals
Oligodeoxyribonucleotides, Antisense
Peptides
Plant Proteins
Reactive Oxygen Species
systemin
Hydrogen Peroxide
Polygalacturonase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Orozco-Cardenas M
Institute of Biological Chemistry, Washington State University, Pullman, WA 99163-6340, USA.
Ryan C A
References (26)
26 references, click to expand
-
Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a NADPH oxidase-like enzyme.
FEBS Lett. 1996 Mar 11;382(1-2):213-7
PMID: 8612756
-
Octadecanoid Precursors of Jasmonic Acid Activate the Synthesis of Wound-Inducible Proteinase Inhibitors.
Plant Cell. 1992 Feb;4(2):129-134
PMID: 12297644
-
Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions.
Plant Cell. 1996 Oct;8(10):1793-1807
PMID: 12239362
-
Disease resistance conferred by expression of a gene encoding H2O2-generating glucose oxidase in transgenic potato plants.
Plant Cell. 1995 Sep;7(9):1357-68
PMID: 8589621
-
Activation of Host Defense Mechanisms by Elevated Production of H2O2 in Transgenic Plants.
Plant Physiol. 1997 Oct;115(2):427-435
PMID: 12223817
-
Proteinase inhibitor-inducing factor activity in tomato leaves resides in oligosaccharides enzymically released from cell walls.
Proc Natl Acad Sci U S A. 1981 Jun;78(6):3536-40
PMID: 16593033
-
Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity.
Cell. 1998 Mar 20;92(6):773-84
PMID: 9529253
-
Structure, expression, and antisense inhibition of the systemin precursor gene.
Science. 1992 Mar 20;255(5051):1570-3
PMID: 1549783
-
Pretreatment of Parsley (Petroselinum crispum L.) Suspension Cultures with Methyl Jasmonate Enhances Elicitation of Activated Oxygen Species.
Plant Physiol. 1994 May;105(1):89-94
PMID: 12232189
-
Nitric oxide functions as a signal in plant disease resistance.
Nature. 1998 Aug 6;394(6693):585-8
PMID: 9707120
-
Systemin potentiates the oxidative burst in cultured tomato cells
Plant Physiol. 1998 Jul;117(3):1031-6
PMID: 9662546
-
An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack.
Plant Cell. 1996 Nov;8(11):2067-77
PMID: 8953771
-
The oxidative burst protects plants against pathogen attack: mechanism and role as an emergency signal for plant bio-defence--a review.
Gene. 1996 Nov 7;179(1):45-51
PMID: 8955628
-
THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE.
Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:251-275
PMID: 15012264
-
A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs.
Plant Cell. 1998 Feb;10(2):255-66
PMID: 9490748
-
Hydrogen Peroxide Stimulates Salicylic Acid Biosynthesis in Tobacco.
Plant Physiol. 1995 Aug;108(4):1673-1678
PMID: 12228572
-
Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesis.
Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):9799-802
PMID: 7937894
-
A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins.
Science. 1991 Aug 23;253(5022):895-7
PMID: 17751827
-
Function of Oxidative Cross-Linking of Cell Wall Structural Proteins in Plant Disease Resistance.
Plant Cell. 1994 Dec;6(12):1703-1712
PMID: 12244231
-
Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway.
Proc Natl Acad Sci U S A. 1995 May 9;92(10):4095-8
PMID: 11607534
-
Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals.
Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12053-8
PMID: 8901530
-
Plasma Membrane Redox Enzyme Is Involved in the Synthesis of O2- and H2O2 by Phytophthora Elicitor-Stimulated Rose Cells.
Plant Physiol. 1995 Apr;107(4):1241-1247
PMID: 12228430
-
Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola.
Plant Cell. 1997 Feb;9(2):209-21
PMID: 9061952
-
Characterization of the Oligogalacturonide-Induced Oxidative Burst in Cultured Soybean (Glycine max) Cells.
Plant Physiol. 1993 May;102(1):233-240
PMID: 12231814
-
Foliar oxidative stress and insect herbivory: Primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance.
J Chem Ecol. 1995 Oct;21(10):1511-30
PMID: 24233680
-
A wound- and systemin-inducible polygalacturonase in tomato leaves.
Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1756-60
PMID: 9990097