The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells

Simon-Plas, Françoise; Elmayan, Taline; Blein, Jean‐Pierre

doi:10.1046/j.1365-313x.2002.01342.x

Cited by 273 publications

(210 citation statements)

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“…ROS production induced in tobacco cells by cryptogein is due to a plasma membrane NADPH oxidase, NtrbohD (Simon-Plas et al, 2002). In this study, we show that transgenic cells inactivated for NtrbohD do not present cryptogeinstimulated clathrin endocytosis, although some other signaling events triggered by the elicitor, such as extracellular alkalinization, are identical to those observed in wild-type cells.…”

Section: Ros Production Is Correlated With Endocytosismentioning

confidence: 54%

“…A BY-2 cell line (named gp3) was previously obtained expressing an antisense construction of NtrbohD cDNA, which is unable to produce ROS when treated with cryptogein, but still responds to the elicitor by an increase in extracellular pH (Simon-Plas et al, 2002) and membrane depolarization (this study; data not shown), similar to wild-type cells.…”

Section: Cryptogein-stimulated Clathrin Endocytosis Is Inhibited In Cmentioning

confidence: 71%

“…To examine whether endocytosis is triggered by ligand-receptor binding and/or by subsequent signaling events, we used a lipid transfer protein (LTP) previously demonstrated to share some structural and plasma membrane-binding properties with elicitins (Blein et al, 2002). In tobacco cells, both cryptogein and an LTP1 from wheat (Triticum aestivum) bind to an identical high-affinity specific site located on the plasma membrane (Buhot et al, 2001).…”

Section: Endocytosis Requires Not Only Binding To the Receptor But Amentioning

confidence: 99%

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The Plant Defense Elicitor Cryptogein Stimulates Clathrin-Mediated Endocytosis Correlated with Reactive Oxygen Species Production in Bright Yellow-2 Tobacco Cells

et al. 2008

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The plant defense elicitor cryptogein triggers well-known biochemical events of early signal transduction at the plasma membrane of tobacco (Nicotiana tabacum) cells, but microscopic observations of cell responses related to these early events were lacking. We determined that internalization of the lipophilic dye FM4-64, which is a marker of endocytosis, is stimulated a few minutes after addition of cryptogein to tobacco Bright Yellow-2 (BY-2) cells. This stimulation is specific to the signal transduction pathway elicited by cryptogein because a lipid transfer protein, which binds to the same receptor as cryptogein but without triggering signaling, does not increase endocytosis. To define the nature of the stimulated endocytosis, we quantified clathrin-coated pits (CCPs) forming on the plasma membrane of BY-2 cells. A transitory stimulation of this morphological event by cryptogein occurs within the first 15 min. In the presence of cryptogein, increases in both FM4-64 internalization and clathrin-mediated endocytosis are specifically blocked upon treatment with 5 mM tyrphostin A23, a receptor-mediated endocytosis inhibitor. The kinetics of the transient increase in CCPs at the plasma membrane coincides with that of transitory reactive oxygen species (ROS) production occurring within the first 15 min after elicitation. Moreover, in BY-2 cells expressing NtrbohD antisense cDNA, which are unable to produce ROS when treated with cryptogein, the CCP stimulation is inhibited. These results indicate that the very early endocytic process induced by cryptogein in tobacco is due, at least partly, to clathrin-mediated endocytosis and is dependent on ROS production by the NADPH oxidase NtrbohD.

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Section: Ros Production Is Correlated With Endocytosismentioning

confidence: 54%

Section: Cryptogein-stimulated Clathrin Endocytosis Is Inhibited In Cmentioning

confidence: 71%

Section: Endocytosis Requires Not Only Binding To the Receptor But Amentioning

confidence: 99%

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The Plant Defense Elicitor Cryptogein Stimulates Clathrin-Mediated Endocytosis Correlated with Reactive Oxygen Species Production in Bright Yellow-2 Tobacco Cells

et al. 2008

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“…Moreover, molecular biology approaches led to the discovery of flavocytochromes of the FRO family that use cytosolic pyridine nucleotides to reduce apoplastic ferrichelates (Robinson et al, 1999). Structurally similar flavocytochromes (Rboh) are involved in one-electron reduction of oxygen with production of superoxide (Simon-Plas et al, 2002). However, these plant flavocytochromes apparently account for a very minor portion of b-type cytochromes associated with the PM, at least under unstressed conditions.…”

Section: Discussionmentioning

confidence: 99%

Auxin-Responsive Genes AIR12 Code for a New Family of Plasma Membrane b-Type Cytochromes Specific to Flowering Plants

et al. 2009

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We report here on the identification of the major plasma membrane (PM) ascorbate-reducible b-type cytochrome of bean (Phaseolus vulgaris) and soybean (Glycine max) hypocotyls as orthologs of Arabidopsis (Arabidopsis thaliana) AIR12 (for auxin induced in root cultures). Soybean AIR12, which is glycosylated and glycosylphosphatidylinositol-anchored to the external side of the PM in vivo, was expressed in Pichia pastoris in a recombinant form, lacking the glycosylphosphatidylinositol modification signal and purified from the culture medium. Recombinant AIR12 is a soluble protein predicted to fold into a b-sandwich domain and belonging to the DOMON (for dopamine b-monooxygenase N terminus) domain superfamily. It is shown to be a b-type cytochrome with a symmetrical a-band at 561 nm, fully reduced by ascorbate, and fully oxidized by monodehydroascorbate radical. AIR12 is a high-potential cytochrome b showing a wide bimodal dependence from the redox potential between +80 mV and +300 mV. Optical absorption and electron paramagnetic resonance analysis indicate that AIR12 binds a single, highly axial low-spin heme, likely coordinated by methionine-91 and histidine-76, which are strongly conserved in AIR12 sequences. Phylogenetic analyses reveal that the auxin-responsive genes AIR12 represent a new family of PM b-type cytochromes specific to flowering plants. Circumstantial evidence suggests that AIR12 may interact with other redox partners within the PM to constitute a redox link between cytoplasm and apoplast.

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“…Similarly, expression of an NADPH oxidase gene (NtRbohD) was also suppressed at 30 u C in TMV-inoculated leaves. NtRbohD encodes an NADPH oxidase shown to be involved in ROS production in tobacco cells treated with the fungal elicitor cryptogein (Simon-Plas et al, 2002). It is likely that the decrease in levels of O 2 $ 2 detected at 30 u C is, at least in part, a consequence of decreased NADPH oxidase gene expression and activity.…”

Section: Discussionmentioning

confidence: 99%

Suppression of tobacco mosaic virus-induced hypersensitive-type necrotization in tobacco at high temperature is associated with downregulation of NADPH oxidase and superoxide and stimulation of dehydroascorbate reductase

Király

Hafez

Fodor

et al. 2008

Journal of General Virology

115

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Tissue necroses and resistance during the hypersensitive response (HR) of tobacco to tobacco mosaic virus (TMV) are overcome at temperatures above 28 6C and the virus multiplies to high levels in the originally resistant N-gene expressing plants. We have demonstrated that chemical compounds that generate reactive oxygen species (ROS) or directly applied hydrogen peroxide (H 2 O 2 ) are able to induce HR-type necroses in TMV-inoculated Xanthi-nc tobacco even at high temperatures (e.g. 30 6C). The amount of superoxide (O 2 $ " ) decreased, while H 2 O 2 slightly increased in TMV-and mock-inoculated leaves at 30 6C, as compared with 20 6C. Activity of NADPH oxidase and mRNA levels of genes that encode NADPH oxidase and an alternative oxidase, respectively, were significantly lower, while activity of dehydroascorbate reductase was significantly higher at 30 6C, as compared with 20 6C. It was possible to reverse or suppress the chemically induced HR-type necrotization at 30 6C by the application of antioxidants, such as superoxide dismutase and catalase, demonstrating that the development of HR-type necroses indeed depends on a certain level of superoxide and other ROS. Importantly, high TMV levels at 30 6C were similar in infected plants, whether the HR-type necrotization developed or not. Suppression of virus multiplication in resistant, HR-producing tobacco at lower temperatures seems to be independent of the appearance of necroses but is associated with temperatures below 28 6C. INTRODUCTIONOne of the best characterized plant-pathogen interactions is the hypersensitive type of resistance (HR) elicited by tobacco mosaic virus (TMV) in tobacco (Nicotiana tabacum). It is known that in the case of the tobacco2 TMV interaction, the HR is governed by the interaction of proteins encoded by the tobacco N (necrosis) gene (Holmes, 1938) and the replicase gene of TMV (Padgett & Beachy, 1993;Padgett et al., 1997). A typical HR is characterized by localized necrotic lesions around the infection sites. It was shown as early as 1931 that tissue necroses associated with the HR of Xanthi-nc tobacco to TMV do not develop at temperatures above 28 u C and the virus multiplies to high levels in the originally resistant N-gene expressing plants (Samuel, 1931). Doke & Ohashi (1988) showed that in TMV-infected Ngene expressing local lesion tobacco hosts, a superoxide (O 2 $ 2 ) generating system is induced. However, this is not the case with systemic hosts lacking the N resistance gene, where virus multiplication and spread are accompanied by non-necrotic symptoms. Furthermore, in a transgenic local lesion host (NahG tobacco) that produces large necrotic lesions upon TMV infection, an increased level of O 2 $ 2 and hydrogen peroxide (H 2 O 2 ) production can be detected at the edge of necrotic spots, as compared with the control non-transgenic tobacco that displays normal-sized lesions (Király et al., 2002). Some investigators claimed that reactive oxygen species (ROS) like O 2 $ 2 and H 2 O 2 could be responsible not only for host cell...

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The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells

Cited by 273 publications

References 57 publications

The Plant Defense Elicitor Cryptogein Stimulates Clathrin-Mediated Endocytosis Correlated with Reactive Oxygen Species Production in Bright Yellow-2 Tobacco Cells

The Plant Defense Elicitor Cryptogein Stimulates Clathrin-Mediated Endocytosis Correlated with Reactive Oxygen Species Production in Bright Yellow-2 Tobacco Cells

Auxin-Responsive Genes AIR12 Code for a New Family of Plasma Membrane b-Type Cytochromes Specific to Flowering Plants

Suppression of tobacco mosaic virus-induced hypersensitive-type necrotization in tobacco at high temperature is associated with downregulation of NADPH oxidase and superoxide and stimulation of dehydroascorbate reductase

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