Abstract
Synthesis of proteinase inhibitor I protein in response to wounding in leaves of excised tomato (Lycopersicon esculentum) plants was inhibited by NO donors sodium nitroprusside and S-nitroso-N-acetyl-penicillamine. The inhibition was reversed by supplying the plants with the NO scavenger 2-(4-carboxiphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide. NO also blocked the hydrogen peroxide (H(2)O(2)) production and proteinase inhibitor synthesis that was induced by systemin, oligouronides, and jasmonic acid (JA). However, H(2)O(2) generated by glucose oxidase and glucose was not blocked by NO, nor was H(2)O(2)-induced proteinase inhibitor synthesis. Although the expression of proteinase inhibitor genes in response to JA was inhibited by NO, the expression of wound signaling-associated genes was not. The inhibition of wound-inducible H(2)O(2) generation and proteinase inhibitor gene expression by NO was not due to an increase in salicylic acid, which is known to inhibit the octadecanoid pathway. Instead, NO appears to be interacting directly with the signaling pathway downstream from JA synthesis, upstream of H(2)O(2) synthesis. The results suggest that NO may have a role in down-regulating the expression of wound-inducible defense genes during pathogenesis.
MeSH Terms
Benzoates/pharmacology
Cyclopentanes/pharmacology
Hydrogen Peroxide/antagonists & inhibitors,metabolism
Imidazoles/pharmacology
Lycopersicon esculentum/drug effects,physiology
Nitric Oxide/physiology
Nitric Oxide Donors/pharmacology
Nitroprusside/pharmacology
Oligosaccharides/pharmacology
Oxylipins
Peptides/pharmacology
Plant Proteins/biosynthesis
S-Nitroso-N-Acetylpenicillamine/pharmacology
Signal Transduction/drug effects
Stress, Mechanical
Chemicals
Benzoates
Cyclopentanes
Imidazoles
Nitric Oxide Donors
Oligosaccharides
Oxylipins
Peptides
Plant Proteins
oligogalacturonic acid
1,3-dihydroxy-4,4,5,5-tetramethyl-2-(4-carboxyphenyl)tetrahydroimidazole
Nitroprusside
Nitric Oxide
systemin
proteinase inhibitor I (plants)
jasmonic acid
S-Nitroso-N-Acetylpenicillamine
Hydrogen Peroxide
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Orozco-Cárdenas Martha L
Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164-6340, USA.
Ryan Clarence A
References (25)
25 references, click to expand
-
Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response.
Proc Natl Acad Sci U S A. 2001 Nov 6;98(23):13454-9
PMID: 11606758
-
Jasmonic acid signaling modulates ozone-induced hypersensitive cell death.
Plant Cell. 2000 Sep;12(9):1633-46
PMID: 11006337
-
Nitric oxide as a signal in plants.
Curr Opin Plant Biol. 1999 Oct;2(5):369-74
PMID: 10508751
-
Nitric oxide and salicylic acid signaling in plant defense.
Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8849-55
PMID: 10922045
-
Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity.
Cell. 1998 Mar 20;92(6):773-84
PMID: 9529253
-
Salicylic Acid Inhibits Synthesis of Proteinase Inhibitors in Tomato Leaves Induced by Systemin and Jasmonic Acid.
Plant Physiol. 1995 Aug;108(4):1741-1746
PMID: 12228577
-
Salicylic acid is not required for Cf-2- and Cf-9-dependent resistance of tomato to Cladosporium fulvum.
Plant J. 2000 Aug;23(3):305-18
PMID: 10929124
-
Data processing for radial immunodiffusion.
Immunochemistry. 1971 Oct;8(10):901-16
PMID: 4339182
-
Nitric oxide functions as a signal in plant disease resistance.
Nature. 1998 Aug 6;394(6693):585-8
PMID: 9707120
-
Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants.
Planta. 2000 Jan;210(2):215-21
PMID: 10664127
-
Quantitative determination of soluble cellular proteins by radial diffusion in agar gels containing antibodies.
Anal Biochem. 1967 Jun;19(3):434-40
PMID: 4963354
-
H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.
Cell. 1994 Nov 18;79(4):583-93
PMID: 7954825
-
THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE.
Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:251-275
PMID: 15012264
-
The systemin signaling pathway: differential activation of plant defensive genes.
Biochim Biophys Acta. 2000 Mar 7;1477(1-2):112-21
PMID: 10708853
-
Role of active oxygen species and NO in plant defence responses.
Curr Opin Plant Biol. 1999 Aug;2(4):287-94
PMID: 10459001
-
Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose.
Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10328-33
PMID: 9707647
-
Redox signaling: nitrosylation and related target interactions of nitric oxide.
Cell. 1994 Sep 23;78(6):931-6
PMID: 7923362
-
Ethylene as a Signal Mediating the Wound Response of Tomato Plants
Science. 1996 Dec 13;274(5294):1914-7
PMID: 8943205
-
Trade-offs between pathogen and herbivore resistance.
Curr Opin Plant Biol. 2000 Aug;3(4):309-14
PMID: 10873851
-
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
-
Nitric oxide assay using hemoglobin method.
Methods Enzymol. 1994;233:240-50
PMID: 8015461
-
Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid.
Mol Plant Microbe Interact. 2000 Mar;13(3):347-51
PMID: 10707361
-
Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate.
Plant Cell. 2001 Jan;13(1):179-91
PMID: 11158538
-
Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway.
Proc Natl Acad Sci U S A. 1999 May 25;96(11):6553-7
PMID: 10339626
-
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