Plasma Membrane Redox Enzyme Is Involved in the Synthesis of O2- and H2O2 by Phytophthora Elicitor-Stimulated Rose Cells

Auh, Chung-Kyoon; Murphy, Terrence M.

doi:10.1104/pp.107.4.1241

Cited by 263 publications

(151 citation statements)

References 34 publications

(45 reference statements)

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“…A Abbreviations: AM, arbuscular mycorrhiza; AMF arbuscular mycorrhizal fungi; APX, ascorbate peroxidase; CAT, catalase; GR, glutathione reductase; GST, glutathione S-transferase; HR, hypersensitive reaction; ROS, reactive oxygen species; SOD, superoxide dismutase. (Auh & Murphy, 1995;Bolwell et al, 1995;Croft et al, 1990;Doke, 1983;Doke & Miura, 1995;Levine et al, 1994).…”

Section: Introductionmentioning

confidence: 99%

Antioxidant enzyme activities in maize plants colonized with Piriformospora indica

et al. 2009

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The bioprotection performance of Piriformospora indica against the root parasite Fusarium verticillioides was studied. We found that maize plants first grown with F. verticillioides and at day 10 inoculated with P. indica showed improvements in biomass, and root length and number as compared with plants grown with F. verticillioides alone. To validate our finding that inoculation with P. indica suppresses colonization by F. verticillioides, we performed PCR analyses using P. indica-and F. verticillioides-specific primers. Our results showed that inoculation with P. indica suppresses further colonization by F. verticillioides. We hypothesized that as the colonization by P. indica increases, the presence of/colonization by F. verticillioides decreases. In roots, catalase (CAT), glutathione reductase (GR), glutathione S-transferase (GST) and superoxide dismutase (SOD) activities were found to be higher in F. verticillioides-colonized plants than in noncolonized plants. Increased activity of antioxidant enzymes minimizes the chances of oxidative burst (excessive production of reactive oxygen species), and therefore F. verticillioides might be protected from the oxidative defence system during colonization. We also observed decreased antioxidant enzyme activities in plants first inoculated with F. verticillioides and at day 10 inoculated with P. indica as compared with plants inoculated with F. verticillioides alone. These decreased antioxidant enzyme activities due to the presence of P. indica help the plant to overcome the disease load of F. verticillioides. We propose that P. indica can be used as a bioprotection agent against the root parasite F. verticillioides. INTRODUCTIONMycorrhizal associations are among the most widespread, intimate and important symbioses in terrestrial ecosystems. Among these, arbuscular mycorrhiza (AM) represent the most ancient and widespread mycorrhizal symbiosis, and are found in a wide range of land plant species (Harrison, 1997). The successful establishment of this mutualistic association constitutes a strategy to fulfil the nutritional demands of both partners . This requires a balance between the defence responses of the host plant and the nutrient demands of the endophyte, resulting in an altered defence-related gene expression, which has been extensively studied during host colonization by obligate biotrophic arbuscular mycorrhizal fungi (AMF). Induction of defence-related genes is most prominent during the early stages of colonization (García-Garrido & Ocampo, 2002), but can also be detected during arbuscule development (Grunwald et al., 2004).The active resistance of plants to colonization by fungi is often expressed by the hypersensitive reaction (HR) of challenged plant cells, and is characterized by reactive oxygen species (ROS), as well as by induced rapid and localized death of plant tissue at the site of infection (Ingram, 1978;Tenhaken et al., 1995). At the biochemical level, the rapid generation of ROS, such as superoxide (O { 2 ) and hydrogen peroxide (H 2 O 2 ), kno...

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Section: Introductionmentioning

confidence: 99%

Antioxidant enzyme activities in maize plants colonized with Piriformospora indica

et al. 2009

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“…H 2 O 2 then can be formed nonenzymatically by dismutation of O 2 Ϫ (25) or enzymatically by the action of SOD (26). To distinguish between the contributions of O 2 Ϫ and H 2 O 2 we analyzed the effects of sodium diethyldithiocarbamate (DDC), an inhibitor of Cu,Zn-SOD (27). DDC blocks H 2 O 2 accumulation in harpin-induced Arabidopsis cells, leading to increased O 2 Ϫ and inhibition of hypersensitive cell death (28).…”

Section: No͞roi Regulation Of Cell Deathmentioning

confidence: 99%

Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response

Delledonne

Zeier

Marocco

et al. 2001

Proc. Natl. Acad. Sci. U.S.A.

969

757

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Nitric oxide (NO) and reactive oxygen intermediates (ROIs) play key roles in the activation of disease resistance mechanisms both in animals and plants. In animals NO cooperates with ROIs to kill tumor cells and for macrophage killing of bacteria. Such cytotoxic events occur because unregulated NO levels drive a diffusionlimited reaction with O 2 ؊ to generate peroxynitrite (ONOO ؊ ), a mediator of cellular injury in many biological systems. Here we show that in soybean cells unregulated NO production at the onset of a pathogen-induced hypersensitive response (HR) is not sufficient to activate hypersensitive cell death. The HR is triggered only by balanced production of NO and ROIs. Moreover, hypersensitive cell death is activated after interaction of NO not with O 2 ؊ but with H 2O2 generated from O2 ؊ by superoxide dismutase. Increasing the level of O 2 ؊ reduces NO-mediated toxicity, and ONOO ؊ is not a mediator of hypersensitive cell death. During the HR, superoxide dismutase accelerates O 2 ؊ dismutation to H2O2 to minimize the loss of NO by reaction with O 2 ؊ and to trigger hypersensitive cell death through NO͞H 2O2 cooperation. However, O2 ؊ rather than H 2O2 is the primary ROI signal for pathogen induction of glutathione S-transferase, and the rates of production and dismutation of O 2 ؊ generated during the oxidative burst play a crucial role in the modulation and integration of NO͞H 2O2 signaling in the HR. Thus although plants and animals use a similar repertoire of signals in disease resistance, ROIs and NO are deployed in strikingly different ways to trigger host cell death.A ttempted infection of plants by an avirulent pathogen elicits a battery of defenses often accompanied by the collapse of challenged host cells. This hypersensitive cell death results in a restricted lesion delimited from surrounding healthy tissue and is thought to contribute to pathogen restriction. An early event in this hypersensitive response (HR) is the generation of superoxide (O 2 Ϫ ) and accumulation of hydrogen peroxide (H 2 O 2 ) in an oxidative burst reminiscent of that producing such reactive oxygen intermediates (ROIs) in activated macrophages (1).Activation of the oxidative burst in the plant HR is part of a highly amplified and integrated signal system that also involves salicylic acid and perturbations of cytosolic Ca 2ϩ to trigger defense mechanisms (2) and to mediate the establishment of systemic immunity (3). The oxidative burst is necessary but not sufficient to trigger host cell death, and recent data indicate that nitric oxide (NO) cooperates with ROIs in the activation of hypersensitive cell death (4).NO and ROIs also interact in the mammalian native immune system where macrophage killing of pathogens and tumor cells involves the diffusion-limited reaction of NO and O 2 to generate ONOO Ϫ , a long lived and highly reactive oxidant species that freely crosses membranes (5), which may modulate NO signal functions (6). ONOO Ϫ induces apoptosis in some human tumor cells (7), and it is also directly cytotoxic...

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“…Incubation of potato tuber slices with an incompatible race of Phytophthora infestans , the potato late blight pathogen, or with a hyphal wall elicitor stimulated NADPH-dependent O 2 Ϫ -generating activity, which was located predominantly in the plasma membrane fraction (Doke, 1985;Doke and Miura, 1995). Diphenylene iodonium, an inhibitor of the phagocyte NADPH oxidase, blocks the oxidative burst in plant cells (Levine et al, 1994;Auh and Murphy, 1995;Piedras et al, 1998). Homologs of gp91 phox (respiratory burst oxidase homolog [ rboh ]), which is the catalytic subunit of phagocyte NADPH oxidase, were isolated from several plants (Groom et al, 1996;Keller et al, 1998;Torres et al, 1998;Amicucci et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

Nicotiana benthamiana gp91^phox Homologs NbrbohA and NbrbohB Participate in H₂O₂ Accumulation and Resistance to Phytophthora infestans

et al. 2003

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Active oxygen species (AOS) are responsible for triggering defense responses in plants. Respiratory burst oxidase homologs ( rboh genes) have been implicated in AOS generation. We have isolated two rboh cDNAs, NbrbohA and NbrbohB , from Nicotiana benthamiana leaves. NbrbohA was expressed constitutively at a low level and the transcripts were increased after mechanical stress of control leaf infiltration, whereas NbrbohB was induced specifically by the protein elicitor INF1 from the potato pathogen Phytophthora infestans . We examined the function of the Nbrboh genes in AOS generation and in the hypersensitive response (HR) using virus-induced gene silencing (VIGS). VIGS indicated that both genes are required for H 2 O 2 accumulation and for resistance to Phytophthora. VIGS of Nbrboh genes also led to a reduction and delay of HR cell death caused by INF1. We further demonstrate that the induction of HR-like cell death by overexpression of a constitutively active mutant of a mitogen-activated protein kinase kinase, MEK DD , is compromised by VIGS of NbrbohB . We found that MEK DD induced NbrbohB but not NbrbohA . This work provides genetic evidence for the involvement of a mitogen-activated protein kinase cascade in the regulation of rboh genes.

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Plasma Membrane Redox Enzyme Is Involved in the Synthesis of O2- and H2O2 by Phytophthora Elicitor-Stimulated Rose Cells

Cited by 263 publications

References 34 publications

Antioxidant enzyme activities in maize plants colonized with Piriformospora indica

Antioxidant enzyme activities in maize plants colonized with Piriformospora indica

Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response

Nicotiana benthamiana gp91^phox Homologs NbrbohA and NbrbohB Participate in H₂O₂ Accumulation and Resistance to Phytophthora infestans

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Plasma Membrane Redox Enzyme Is Involved in the Synthesis of O2- and H2O2 by Phytophthora Elicitor-Stimulated Rose Cells

Cited by 263 publications

References 34 publications

Antioxidant enzyme activities in maize plants colonized with Piriformospora indica

Antioxidant enzyme activities in maize plants colonized with Piriformospora indica

Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response

Nicotiana benthamiana gp91phox Homologs NbrbohA and NbrbohB Participate in H2O2 Accumulation and Resistance to Phytophthora infestans

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Nicotiana benthamiana gp91^phox Homologs NbrbohA and NbrbohB Participate in H₂O₂ Accumulation and Resistance to Phytophthora infestans