Ozone‐induced cell death occurs via two distinct mechanisms in <i>Arabidopsis</i>: the role of salicylic acid

Rao, Mulpuri V.; Davis, Keith

doi:10.1046/j.1365-313x.1999.00400.x

Cited by 437 publications

(373 citation statements)

References 40 publications

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“…Our findings and model concerning the roles of RBOHD-derived ROS in the regulation of A. brassicicolainduced plant cell death represent a refinement of a concept suggested previously (Levine et al, 1994;Rao and Davis, 1999;Vandenabeele et al, 2003). ROS produced by plant cells under stress possess dual, concentration-dependent functions.…”

Section: Rbohd Interplays With Sa and Et In The Regulation Of Cell Deathsupporting

confidence: 70%

Dual Roles of Reactive Oxygen Species and NADPH Oxidase RBOHD in an Arabidopsis-Alternaria Pathosystem

et al. 2009

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Arabidopsis (Arabidopsis thaliana) NADPH oxidases have been reported to suppress the spread of pathogen- and salicylic acid-induced cell death. Here, we present dual roles of RBOHD (for respiratory burst oxidase homolog D) in an Arabidopsis-Alternaria pathosystem, suggesting either initiation or prevention of cell death dependent on the distance from pathogen attack. Our data demonstrate that a rbohD knockout mutant exhibits increased spread of cell death at the macroscopic level upon inoculation with the fungus Alternaria brassicicola. However, the cellular patterns of reactive oxygen species accumulation and cell death are fundamentally different in the AtrbohD mutant compared with the wild type. Functional RBOHD causes marked extracellular hydrogen peroxide accumulation as well as cell death in distinct, single cells of A. brassicicola-infected wild-type plants. This single cell response is missing in the AtrbohD mutant, where infection triggers spreading-type necrosis preceded by less distinct chloroplastic hydrogen peroxide accumulation in large clusters of cells. While the salicylic acid analog benzothiadiazole induces the action of RBOHD and the development of cell death in infected tissues, the ethylene inhibitor aminoethoxyvinylglycine inhibits cell death, indicating that both salicylic acid and ethylene positively regulate RBOHD and cell death. Moreover, A. brassicicola-infected AtrbohD plants hyperaccumulate ethylene and free salicylic acid compared with the wild type, suggesting negative feedback regulation of salicylic acid and ethylene by RBOHD. We propose that functional RBOHD triggers death in cells that are damaged by fungal infection but simultaneously inhibits death in neighboring cells through the suppression of free salicylic acid and ethylene levels.

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Section: Rbohd Interplays With Sa and Et In The Regulation Of Cell Deathsupporting

confidence: 70%

Dual Roles of Reactive Oxygen Species and NADPH Oxidase RBOHD in an Arabidopsis-Alternaria Pathosystem

et al. 2009

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“…An RNA blot was prepared with 32 Arabidopsis, in CaM-mediated cell death. We demonstrate that (i) oxidative stress, involved in plant PCD processes, [40][41][42][43] induces the transient expression of AtBAG6, (ii) AtBAG6 physically interacts with AtCaMs, (iii) the IQ motif in the AtBAG6 is required for Ca 2 þ -independent CaM complex formation, and (iv) the CaM-binding IQ motif and BAG domain are required for AtBAG6-mediated cell death in both yeast and plant. In animals, Ca 2 þ released into the cytoplasm can induce mitochondrial permeability transition (PT) pore opening, which induces release of apoptotic activators to the cytoplasm and consequently activates caspase-mediated PCD.…”

Section: Discussionmentioning

confidence: 86%

“…ROS are utilized as second messengers in the execution of cell death during hypersensitivity responses and ozone-mediated cell death -well-studied plant PCD phenomenona that are induced by biotic and abiotic stress, respectively. 42 Similarly, AtBAG6-induced cell death in Arabidopsis and yeast is also mediated by ROS generation (Figures 4 and 8). Therefore, it would appear that ROS is a common element and key event of PCD in animals, plants, and yeast, where it is a common component of a basic, evolutionarily conserved mechanism.…”

Section: Discussionmentioning

confidence: 90%

“…Transcription of AtBAG6 was specifically induced by SA, H 2 O 2 , and high temperature, all of which are known to be involved in plant PCD processes. [40][41][42][43] To further determine the biological roles of AtBAG6 in plants, we constructed each plasmid containing CDD or CDD I575S under the control of the constitutive cauliflower mosaic virus 35S promoter using the pCAMBIA1302 binary vector and used these plasmids to transform Arabidopsis. Transgenic CDD plants showed midget (dwarfism) phenotypes and formed disease-like necrotic lesions on their leaves (Figure 9b and c).…”

Section: Induction Of Cell Death By Atbag6 In Arabidopsis Plantmentioning

confidence: 99%

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AtBAG6, a novel calmodulin-binding protein, induces programmed cell death in yeast and plants

et al. 2005

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Calmodulin (CaM) influences many cellular processes by interacting with various proteins. Here, we isolated AtBAG6, an Arabidopsis CaM-binding protein that contains a central BCL-2-associated athanogene (BAG) domain. In yeast and plants, overexpression of AtBAG6 induced cell death phenotypes consistent with programmed cell death (PCD). Recombinant AtBAG6 had higher affinity for CaM in the absence of free Ca 2 þ than in its presence. An IQ motif (IQXXXRGXXXR, where X denotes any amino-acid) was required for Ca 2 þ -independent CaM complex formation and single amino-acid changes within this motif abrogated both AtBAG6-activated CaM-binding and cell death in yeast and plants. A 134-amino-acid stretch, encompassing both the IQ motif and BAG domain, was sufficient to induce cell death. Agents generating oxygen radicals, which are known to be involved in plant PCD, specifically induced the AtBAG6 transcript. Collectively, these results suggest that AtBAG6 is a stress-upregulated CaM-binding protein involved in plant PCD.

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“…SA acts as a hormone in plant processes like thermogenesis (Raskin et al, 1987), ethylene synthesis, and fruit ripening (Leslie and Romani, 1988), but it also acts as a stress regulator during plant defense response (Rao and Davis, 1999;Senaratna et al, 2000;Yalpani et al, 1991). Accumulation of SA is often correlated with an increase in ROS production during plant stress response (for review, see Herrera-Vásquez et al, 2015).…”

mentioning

confidence: 99%

Salicylic Acid-Dependent Plant Stress Signaling via Mitochondrial Succinate Dehydrogenase

et al. 2017

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Mitochondria are known for their role in ATP production and generation of reactive oxygen species, but little is known about the mechanism of their early involvement in plant stress signaling. The role of mitochondrial succinate dehydrogenase (SDH) in salicylic acid (SA) signaling was analyzed using two mutants: disrupted in stress response1 (dsr1), which is a point mutation in SDH1 identified in a loss of SA signaling screen, and a knockdown mutant (sdhaf2) for SDH assembly factor 2 that is required for FAD insertion into SDH1. Both mutants showed strongly decreased SA-inducible stress promoter responses and low SDH maximum capacity compared to wild type, while dsr1 also showed low succinate affinity, low catalytic efficiency, and increased resistance to SDH competitive inhibitors. The SA-induced promoter responses could be partially rescued in sdhaf2, but not in dsr1, by supplementing the plant growth media with succinate. Kinetic characterization showed that low concentrations of either SA or ubiquinone binding site inhibitors increased SDH activity and induced mitochondrial H 2 O 2 production. Both dsr1 and sdhaf2 showed lower rates of SA-dependent H 2 O 2 production in vitro in line with their low SA-dependent stress signaling responses in vivo. This provides quantitative and kinetic evidence that SA acts at or near the ubiquinone binding site of SDH to stimulate activity and contributes to plant stress signaling by increased rates of mitochondrial H 2 O 2 production, leading to part of the SA-dependent transcriptional response in plant cells.

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Ozone‐induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid

Cited by 437 publications

References 40 publications

Dual Roles of Reactive Oxygen Species and NADPH Oxidase RBOHD in an Arabidopsis-Alternaria Pathosystem

Dual Roles of Reactive Oxygen Species and NADPH Oxidase RBOHD in an Arabidopsis-Alternaria Pathosystem

AtBAG6, a novel calmodulin-binding protein, induces programmed cell death in yeast and plants

Salicylic Acid-Dependent Plant Stress Signaling via Mitochondrial Succinate Dehydrogenase

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