Sensing and Signalling in Response to Oxygen Deprivation in Plants and Other Organisms

Bailey‐Serres, Julia; Chang, Ruth

doi:10.1093/aob/mci206

Cited by 226 publications

(160 citation statements)

References 116 publications

(160 reference statements)

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“…Hence, mitochondrial ROS are likely to accumulate in harpin-elicited leaves under VLO and might contribute to the higher cell death rates. These results are in good agreement with the hypothesis that the mitochondrial ETC acts as an oxygen sensor such that mitochondria are able to detect oxygen deprivation (72,73). In contrast, the accumulation of ROS in the chloroplasts seems to be less important, since both DAB and NBT staining are prevented under VLO (Fig.…”

Section: Oxygen Deprivation Interferes With the Pcd Process By Limitisupporting

confidence: 90%

“…Our data also challenge the roles for apoplastic ROS produced by plasmamembrane NADPH oxidases and peroxidases in the execution of cell death. These enzymes are involved in ROS generation during mild hypoxic stress (72,74). However, the conditions of severe oxygen deprivation applied here (Ͻ0.1% O 2 ) should markedly repress NADPH oxidase activity, which has a K m of around 5-10 M (corresponding to 0.2-0.5% O 2 ) (75).…”

Section: Oxygen Deprivation Interferes With the Pcd Process By Limitimentioning

confidence: 99%

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Light and Oxygen Are Not Required for Harpin-induced Cell Death

Garmier

Priault²,

Vidal³

et al. 2007

Journal of Biological Chemistry

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Nicotiana sylvestris leaves challenged by the bacterial elicitor harpin N Ea were used as a model system in which to determine the respective roles of light, oxygen, photosynthesis, and respiration in the programmed cell death response in plants. The appearance of cell death markers, such as membrane damage, nuclear fragmentation, and induction of the stress-responsive element Tnt1, was observed in all conditions. However, the cell death process was delayed in the dark compared with the light, despite a similar accumulation of superoxide and hydrogen peroxide in the chloroplasts. In contrast, harpin-induced cell death was accelerated under very low oxygen (<0.1% O 2 ) compared with air. Oxygen deprivation impaired accumulation of chloroplastic reactive oxygen species (ROS) and the induction of cytosolic antioxidant genes in both the light and the dark. It also attenuates the collapse of photosynthetic capacity and the respiratory burst driven by mitochondrial alternative oxidase activity observed in air. Since alternative oxidase is known to limit overreduction of the respiratory chain, these results strongly suggest that mitochondrial ROS accumulate in leaves elicited under low oxygen. We conclude that the harpin-induced cell death does not require ROS accumulation in the apoplast or in the chloroplasts but that mitochondrial ROS could be important in the orchestration of the cell suicide program.Light and oxygen are generally considered to be important in the responses of plants to environmental stress, principally because they are involved in the generation of reactive oxygen species (ROS) 4 and associated molecular and biochemical changes. ROS are central to redox sensing during biotic and abiotic stress responses, and they act as second messengers in the activation of signal transduction pathways. ROS activate mitogen-activated protein kinase cascades that phosphorylate a variety of proteins involved in plant growth and development as well as death responses (1). High ROS levels can trigger the appearance of programmed cell death (PCD) and the induction of caspase activation in animals (2) and the activation of the ubiquitin/26 S proteasome system in plants (3). The cellular compartmentation of ROS production in PCD responses has been extensively investigated. For example, it has been established that ROS are generated in the apoplast during the oxidative burst that often accompanies plant PCD responses (4). It is widely accepted that this oxidative burst is caused by activation of DPI-sensitive NADPH oxidase-like enzymes (5) and/or the activation of various extracellular oxidases and peroxidases (6) linked to the spontaneous or enzyme-catalyzed dismutation of superoxide to H 2 O 2 . However, clear cause and effect relationships between apoplastic ROS production and the execution of cell death have never been established, and ROS have been suggested to be involved in the spread of cell death rather than in the death process per se (7).Other possible sites of ROS production are the chloroplasts and mitochond...

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Section: Oxygen Deprivation Interferes With the Pcd Process By Limitisupporting

confidence: 90%

Section: Oxygen Deprivation Interferes With the Pcd Process By Limitimentioning

confidence: 99%

Light and Oxygen Are Not Required for Harpin-induced Cell Death

Garmier

Priault²,

Vidal³

et al. 2007

Journal of Biological Chemistry

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“…Secondary signaling molecules to monitor O 2 availability might relay on calcium flux, energy charge, and ROS balance. These three parameters seem to be interrelated, thus suggesting the presence of downstream events that could converge (Bailey-Serres and Chang, 2005). Emerging evidence suggests that ROS-mediated activation of plasma membrane calcium (Ca 2+ ) channels is involved in plant signal transduction related to both biotic and abiotic stress and development events (for review, see Lecourieux et al, 2006).…”

Section: Resultsmentioning

confidence: 99%

Reactive Oxygen Species-Driven Transcription in Arabidopsis under Oxygen Deprivation

et al. 2012

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Reactive oxygen species (ROS) play an important role as triggers of gene expression during biotic and abiotic stresses, among which is low oxygen (O 2 ). Previous studies have shown that ROS regulation under low O 2 is driven by a RHO-like GTPase that allows tight control of hydrogen peroxide (H 2 O 2 ) production. H 2 O 2 is thought to regulate the expression of heat shock proteins, in a mechanism that is common to both O 2 deprivation and to heat stress. In this work, we used publicly available Arabidopsis (Arabidopsis thaliana) microarray datasets related to ROS and O 2 deprivation to define transcriptome convergence pattern. Our results show that although Arabidopsis response to anoxic and hypoxic treatments share a common core of genes related to the anaerobic metabolism, they differ in terms of ROS-related gene response. We propose that H 2 O 2 production under O 2 deprivation is a trait present in a very early phase of anoxia, and that ROS are needed for the regulation of a set of genes belonging to the heat shock protein and ROS-mediated groups. This mechanism, likely not regulated via the N-end rule pathway for O 2 sensing, is probably mediated by a NADPH oxidase and it is involved in plant tolerance to the stress.

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“…Indirect low-oxygen sensing is thought to involve the perception of dynamics in levels of adenylates, carbohydrates, and pyruvate as well as localized cellular changes in pH, Ca 2+ , ROS, and nitric oxide (NO; Bailey-Serres and Chang, 2005;Rhoads and Subbaiah, 2007;Bailey-Serres and Voesenek 2008;Blokhina and Fagerstedt, 2010). The decline in adenylates or carbohydrates is likely to trigger SnRK1-regulated carbon management (Baena-González, 2010).…”

Section: Indirect Sensingmentioning

confidence: 99%