Effects ofErwinia amylovoraharpin on tobacco leaf cell membranes are related to leaf necrosis and electrolyte leakage and distinct from perturbations caused by inoculatedE. amylovora

Pike, Sharon; Ádám, Attila L.; Pu, Xin-An; Hoyos, Mary Elizabeth; Laby, Ron J.; Beer, Steven V.; Novacký, A.

doi:10.1006/pmpp.1998.0167

Cited by 47 publications

(51 citation statements)

References 29 publications

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“…Similarly, in previous work, irreversible depolarization was an early characteristic of both HR that is associated with species level resistance to a broad range of pathogens (Keppler and Novacky, 1986;Pavlovkin and Novacky, 1986;Pike et al, 1998) and HR-like necrosis that was caused by harpin Ea (Pike et al, 1998). In the first case, multiple external and internal bacterial effectors likely led to electrolyte leakage and confluent necrosis.…”

Section: Discussionsupporting

confidence: 59%

“…Because all these ion fluxes are down the chemical gradient, they would occur as a direct consequence of membrane depolarization caused by membrane damage or H 1 -ATPase down-regulation, and do not necessarily constitute a specific signal. Membrane damage or unregulated H 1 -ATPase malfunction can probably be ruled out as the source of early membrane depolarization because the fungal toxin fusicoccin always hyperpolarized even very depolarized membranes (data not shown), as found previously with bacterial HR (Pavlovkin and Novacky, 1986) and harpin (Popham et al, 1995;Pike et al, 1998). Fusicoccin locks the H 1 -ATPase in the active position, resulting in hyperpolarization when the H 1 -ATPase is functional and the membrane is capable of separating charge (Sze et al, 1999;Bunney et al, 2002).…”

Section: The Significance Of Membrane Depolarizationsupporting

confidence: 63%

“…4) and even for 24 h (data not shown). In previous work, LaCl 3 prevented tissue collapse, electrolyte leakage, and depolarization caused by harpin Ea (He et al, 1994;Pike et al, 1998). LaCl 3 also prevented an increase in cytosolic calcium and H 2 O 2 , and HR in Arabidopsis leaves when coinfiltrated with bacteria expressing avrRpm1 (Grant et al, 2000).…”

Section: The Significance Of Membrane Depolarizationmentioning

confidence: 75%

“…harpin, and advances in molecular techniques have made it possible to investigate signaling and related plant membrane responses during HR. Ion fluxes were observed immediately after harpin from Erwinia amylovora (harpin Ea ) was applied to tobacco (Nicotiana tabacum) suspension cells (Baker et al, 1993), and the membrane potential depolarized just minutes after harpin Ea was added to the bath solution surrounding suspension cells (Popham et al, 1995) or leaf segments (Pike et al, 1998). Depolarization patterns distinguished between leaves from plants that underwent HR and those that did not collapse (Pike et al, 1998).…”

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confidence: 99%

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Electrophysiological Characterization of the Arabidopsis avrRpt2-Specific Hypersensitive Response in the Absence of Other Bacterial Signals

2005

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The hypersensitive response (HR) is defined as rapid cell collapse at the infection site and often accompanies plant resistance. The physiological processes leading to HR are not well understood. Here, we report an electrophysiological characterization of bacterial HR caused by a single avirulence gene in the absence of other bacterial signals. We used dexamethasone (dex)-inducible transgenic Arabidopsis (Arabidopsis thaliana) plants containing the avrRpt2 gene from Pseudomonas syringae pv tomato. Membrane depolarization in these plants began 1 to 1.5 h after dex application, hours before electrolyte leakage. Progressive depolarization was a sensitive early indicator of HR that occurred only in Arabidopsis leaf cells expressing both avrRpt2 and a functional RPS2 gene. Hyperpolarization of fully depolarized membranes by fusicoccin, a fungal toxin that activates the H 1 -ATPase, indicates that depolarization did not result from a nonfunctional pump or leaky membranes. Depolarization and electrolyte leakage were inhibited in RPS2 plants by the calcium channel blocker LaCl 3 , highly correlating these events and suggesting that Ca 21 entry into cells is required for both. Also correlated were inhibition of depolarization, electrolyte leakage, and HR following salicylic acid pretreatment. In salicylic acid-pretreated RPS2 seedlings, avrRpt2 transcript was produced after dex treatment. However, AvrRpt2 protein accumulation was greatly reduced, suggesting a possible mechanism for inhibition of HR in plants with induced resistance. This experimental system is a very sensitive assay that lends itself to the dissection of physiological processes leading to HR in plants, and provides a baseline for future research within a genetic framework.Plants are resistant to infection by many pathogens. Plants expressing a resistance (R) gene rapidly initiate defense responses following contact with a pathogen that expresses a corresponding avirulence (avr) gene (Flor, 1971). Isogenic plants lacking the R gene fall prey to the pathogen. The hypersensitive response (HR), rapid cell collapse at the site of infection, is often dramatic evidence of resistance, particularly in bacteriainduced HR (Goodman and Novacky, 1994;Heath, 2000).Many defense responses associated with bacteriainduced HR have been described since Klement et al. (1964) first demonstrated the total collapse of nonhost plant leaves following infiltration of pathogenic bacteria. They include ion fluxes, increased salicylic acid (SA) production, membrane depolarization, and pathogenesis-related (PR) gene induction (Goodman and Novacky, 1994;Dangl et al., 1996; HammondKosack and Jones, 1996;Dangl and Jones, 2001). Yet, the mechanism of HR induction is not well understood.The functional significance of bacteria-induced HR also is not clear because defense responses and resistance can occur without HR. For example, systemically acquired resistance, resistance to a broad spectrum of pathogens, can be induced in normally susceptible plants by pathogen infection or application o...

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Section: Discussionsupporting

confidence: 59%

Section: The Significance Of Membrane Depolarizationsupporting

confidence: 63%

Section: The Significance Of Membrane Depolarizationmentioning

confidence: 75%

mentioning

confidence: 99%

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Electrophysiological Characterization of the Arabidopsis avrRpt2-Specific Hypersensitive Response in the Absence of Other Bacterial Signals

2005

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“…Some differences between HR and mammalian apoptosis were observed, however, such as changes in DNA laddering (5,8) and the lack in HR of the repressor role of Bcl-x L (12). One ultimate characteristic of HR is the loss of membrane integrity, and thus HR is often characterized by an associated electrolyte leakage (5,13). This feature is not encountered in mammalian apoptosis but is one characteristic of the catastrophic cell death called necrosis, which is not dependent on gene activation (14).…”

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confidence: 99%

Involvement of Lipoxygenase-dependent Production of Fatty Acid Hydroperoxides in the Development of the Hypersensitive Cell Death induced by Cryptogein on Tobacco Leaves

Rustérucci¹,

Montillet²,

Agnel³

et al. 1999

Journal of Biological Chemistry

218

212

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Lipid peroxidation was investigated in relation with the hypersensitive reaction in cryptogein-elicited tobacco leaves. A massive production of free polyunsaturated fatty acid (PUFA) hydroperoxides dependent on a 9-lipoxygenase (LOX) activity was characterized during the development of leaf necrosis. The process occurred after a lag phase of 12 h, was accompanied by the concomitant increase of 9-LOX activity, and preceded by a transient accumulation of LOX transcripts. Free radical-mediated lipid peroxidation represented 10% of the process. Inhibition and activation of the LOX pathway was shown to inhibit or to activate cell death, and evidence was provided that fatty acid hydroperoxides are able to mimic leaf necrotic symptoms. Within 24 h, about 50% of leaf PUFAs were consumed, chloroplast lipids being the major source of PUFAs. The results minimize the direct participation of active oxygen species from the oxidative burst in membrane lipid peroxidation. They suggest, furthermore, the involvement of lipase activity to provide the free PUFA substrates for LOX. The LOX-dependent peroxidative pathway, responsible for tissue necrosis, appears as being one of the features of hypersensitive programmed cell death.In plant-pathogen interactions, a typical feature of plant resistance is hypersensitive reaction (HR), 1 characterized by the induction of rapid cell death at the site of an attempted attack by either an avirulent strain of a pathogen or a nonpathogen. The collapse of challenged cells, occurring during incompatible interactions, was shown in most cases to be dependent on a gene for gene plant pathogen interaction (1, 2). HR is accompanied by a battery of defense mechanisms including de novo synthesis of antimicrobial enzymes and metabolites, strengthening of the cell wall, and the onset of systemic acquired resistance dependent on salicylic acid accumulation (3, 4). HR often leads to dry lesions that are supposed to limit pathogen growth. Other proposed roles is the release in apoplasm of defense-related proteins and toxic metabolites, as well as of signals that activate the defenses of both neighboring and distant cells. Hypersensitive cell death appears to not be the result of the direct action of released pathogenic factors but is rather under the genetic control of the host. Indeed, several observations underline that HR is an example of PCD in plants (1, 2). Furthermore, hypersensitive cell death has morphological and molecular features similar to the mammalian PCD, called apoptosis. These include cytoplasm and chromatin condensation followed by their fragmentation, activation of calciumdependent endonucleases (5-8) and of cysteine proteases (9 -11), and involvement of similar regulation factors (2). Some differences between HR and mammalian apoptosis were observed, however, such as changes in DNA laddering (5,8) and the lack in HR of the repressor role of Bcl-x L (12). One ultimate characteristic of HR is the loss of membrane integrity, and thus HR is often characterized by an associated electrolyte le...

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Local early induced resistance of plants as the first line of defence against bacteria

Klement

Bozsó

Kecskés

et al. 2003

Pest Management Science

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This paper is an overview of a non-specific local early induced resistance (EIR) mechanism, distinct from the incompatible-specific hypersensitive reaction (HR). We have shown that the local induced resistance (LIR) described earlier is not a single and uniform response to pathogen infection, because an early (EIR) and a late form can be distinguished. EIR operates from 3-6 h post-inoculation (hpi) until about 20 hpi, and is inhibited by a short heat-shock or the eukaryotic protein synthesis inhibitor, cycloheximide. In contrast, LIR, which corresponds to the induced resistance forms discovered earlier, requires more time (about 24 h) and intensive illumination to develop, and is effective for a longer period. EIR develops parallel with HR and is sometimes able to prevent it when the induction time of HR is longer than the time required for the development of EIR. It seems that EIR inhibits the metabolism of bacteria and the activity of hrp genes which otherwise are required for the induction of HR. In a compatible host-pathogen relationship the effect of EIR fails to take place. The rapid development of EIR is greatly influenced by temperature and the physiological state of the plant. EIR activates the accumulation of hydrogen peroxide at the bacterial attachment, expressing new peroxidase isoenzymes in the initiated plant tissue. It seems that this is a native general local defence mechanism which can localise foreign organisms even at the penetration site.

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Effects ofErwinia amylovoraharpin on tobacco leaf cell membranes are related to leaf necrosis and electrolyte leakage and distinct from perturbations caused by inoculatedE. amylovora

Cited by 47 publications

References 29 publications

Electrophysiological Characterization of the Arabidopsis avrRpt2-Specific Hypersensitive Response in the Absence of Other Bacterial Signals

Electrophysiological Characterization of the Arabidopsis avrRpt2-Specific Hypersensitive Response in the Absence of Other Bacterial Signals

Involvement of Lipoxygenase-dependent Production of Fatty Acid Hydroperoxides in the Development of the Hypersensitive Cell Death induced by Cryptogein on Tobacco Leaves

Local early induced resistance of plants as the first line of defence against bacteria

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