Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance?

Neuenschwander, Urs; Vernooij, Bernard; Friedrich, Leslie; Uknes, Scott; Keßmann, Helmut; Ryals, John

doi:10.1046/j.1365-313x.1995.08020227.x

Cited by 212 publications

(146 citation statements)

References 29 publications

(37 reference statements)

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“…Careful analysis of SA-binding to plant proteins using SA with a specific activity that is normally used in receptor-binding studies, would have shown that more iron-containing enzymes than catalase bind SA. Most recently, independent experiments have been conducted showing also that the concept of elevated levels of H202 [9] as a consequence of possible catalase inhibition by SA is not required for systemic acquired resistance [23] and that H202 does not function downstream of SA in the induction of PR protein expression [24]. Furthermore, it has previously been shown that SA is essential for the development of systemic asquired resistance [25] but that the systemic acquired resistance inducing signal is not SA [26].…”

Section: Discussionmentioning

confidence: 99%

Evidence against specific binding of salicylic acid to plant catalase

1995

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It was demonstrated that salicylic acid (SA) not only binds to catalase from differentiated higher plants and plant cell suspension cultures but also to those of fungi and animals. SA bound specifically to iron-containing enzymes, such as catalase, aconitase, lipoxidase and peroxidase, while not to iron-free plant enzymes. On the grounds of these experiments, the claim is further challenged that SA is a signalling compound and second messenger in plants that activates plant defense-related genes through elevated H202 levels by specifically inhibiting catalase activity. SA may just function as a phytoalexin.

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Section: Discussionmentioning

confidence: 99%

Evidence against specific binding of salicylic acid to plant catalase

1995

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“…This amplification may reflect a runaway cycle where SA and ROIs are involved. Indeed H 2 O 2 can induce SA synthesis (Leo Â n et al, 1995;Neuenschwander et al, 1995) which, at very high concentrations, can inhibit catalase and other scavenging enzymes (Chen et al, 1993), potentiating further accumulation of H 2 O 2 (Shirasu et al, 1997).…”

Section: Is There a Social Role For The Hr?mentioning

confidence: 99%

The hypersensitive response and the induction of cell death in plants

1997

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The hypersensitive response, or HR, is a form of cell death often associated with plant resistance to pathogen infection. Reactive oxygen intermediates and ion fluxes are proximal responses probably required for the HR. Apoptosis as defined in animal systems is, thus far, not a strict paradigm for the HR. The diversity observed in plant cell death morphologies suggests that there may be multiple pathways through which the HR can be triggered. Signals from pathogens appear to interfere with these pathways. HR may play in plants the same role as certain programmed cell deaths in animals with respect to restricting pathogen growth. In addition, the HR could regulate the defense responses of the plant in both local and distant tissues.

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“…The suggestion that SA-dependent inhibition of APX in planta may result in the elevation of H 2 O 2 levels, which in turn acts as a second messenger in SAR signaling (15), is therefore not tenable. Neuenschwander et al (17) reported that no increase of H 2 O 2 in tobacco mosaic virus-infected tobacco plants is found during the onset of SAR (17). In addition hydrogen peroxide does not function downstream of SA (11).…”

Section: Sa Is Not An Inhibitor Of Apx-mentioning

confidence: 98%

Section: This Communication Describes the Interactions Of Salicylic Amentioning

confidence: 99%

“…In addition, while the irreversible catalase inhibitor 3-amino-1,2,4-triazole was found to be a weak inducer of PR-1 expression relative to SA in wild-type tobacco, it was unable to induce PR-1 in nahG transformed plants. This suggests that the action of PR-1 depends on the accumulation of SA but not necessarily on the inhibition of catalase (11,17).The present communication is concerned with the interactions of SA with APX in vitro. APX with ascorbic acid (AsA) as a reducing substrate is believed to scavenge excess H 2 O 2 formed in plants under both stress and normal conditions (18,19).…”

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confidence: 90%

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Salicylic Acid Is a Reducing Substrate and Not an Effective Inhibitor of Ascorbate Peroxidase

Kvaratskhelia¹,

George

Thorneley

1997

Journal of Biological Chemistry

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This communication describes the interactions of salicylic acid (SA) with plant ascorbate peroxidase (APX).Contrary to a recent report (Durner, J., and Klessig, D. F. (1995) Proc. Natl. Acad. Sci. U. S. A. 92, 11312-11316) we show conclusively that ascorbate oxidation by APX is not inhibited by SA (10 mM), but that SA is a slow reducing substrate of this enzyme. The suggestion that SA-dependent inhibition of APX in planta may result in the elevation of H 2 O 2 levels, which in turn acts as a second messenger in systemic acquired resistance signaling, is therefore not tenable. We conclude that APX remains a key antioxidant during systemic acquired resistance following pathogenic infection of plants. The transient products of SA oxidation by APX appear to be SA free radicals that undergo subsequent chemistry. APX-dependent oxidation of SA could be essential for diminishing the detrimental effects of this phenolic acid on plant cells.Salicylic acid (2-hydroxybenzoic acid) is believed to play an important role in plant defense responses against pathogen attack (see Refs. 1 and 2 and references therein). Many studies implicate SA 1 as an essential signal in the development of the systemic acquired resistance (SAR) in several plant species. SAR is an inducible, long lasting, broad-based pathogen defense mechanism following infection of plants, particularly by a necrotizing pathogen. An understanding of the molecular basis of SAR may well lead to the development of both genetically engineered crops with enhanced disease resistance and novel chemicals that stimulate the plants' resistance to pathogens.Although induction of SAR is associated with a significant increase in endogenous SA levels in plants (3, 4), the biochemical basis of this phenomenon is obscure. SA accumulation is essential for pathogenesis-related (PR) gene expression (5, 7). Exogenous application of SA to Arabidopsis or tobacco switches on the same set of SAR genes as pathogen infection and induces protection against the same spectrum of pathogens (5,8). Experiments with transgenic plants that express a bacterial salicylate hydroxylase gene have shown that SA could be a transmissible signal (9). The constitutive expression of salicylate hydroxylase, encoded by the nahG gene from Pseudomonas putida, prevented the accumulation of SA in transgenic tobacco by converting it to catechol, which is inactive in SAR. Treatment of nahG plants with tobacco mosaic virus did not induce SAR (9) or SAR gene expression in systemic leaves (10). Grafting experiments involving nahG and wild-type tobacco have suggested that although SA is probably not a long distance signal, its presence in systemic tissue is absolutely required for PR protein expression and establishment of SAR (10). PR-1a gene expression in infected tissues is dependent on SA accumulation and supports the suggestion that at least local induction of this PR protein operates via salicylate signaling (11).Klessig and co-workers (12-14) have suggested that one mechanism of SA action is to inhibit catalase an...

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Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance?

Cited by 212 publications

References 29 publications

Evidence against specific binding of salicylic acid to plant catalase

Evidence against specific binding of salicylic acid to plant catalase

The hypersensitive response and the induction of cell death in plants

Salicylic Acid Is a Reducing Substrate and Not an Effective Inhibitor of Ascorbate Peroxidase

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