Respiratory burst oxidases: the engines of ROS signaling

Suzuki, Nobuhiro; Miller, Gad; Morales, Jairo; Shulaev, Vladimir; Torres, Miguel Ángel Medina; Mittler, Ron

doi:10.1016/j.pbi.2011.07.014

Cited by 867 publications

(641 citation statements)

References 60 publications

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“…Moreover, transient changes in Ca 2+ during low O 2 was found to be involved in ADH regulation (Sedbrook et al, 1996;Subbaiah et al, 1994aSubbaiah et al, , 1994b. A connection between NADPH-oxidase-dependent ROS production and Ca 2+ oscillation has been suggested in Arabidopsis, where Ca 2+ likely binds to the EF hands of the N-terminal region of NADPH oxidase and, together with phosphorylation, promotes ROS production (Ogasawara et al, 2008;Takeda et al, 2008;Suzuki et al, 2011). Whether and how this mechanism could in part overlap with N-end rule pathway is still unknown.…”

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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Section: Resultsmentioning

confidence: 99%

Reactive Oxygen Species-Driven Transcription in Arabidopsis under Oxygen Deprivation

et al. 2012

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“…Nonetheless, the accumulation of superoxide and H 2 O 2 is readily detected in local or systemic wounded tissue (Sagi et al, 2004;Warwar et al, 2011) and in the immune responses (Dubiella et al, 2013). A possible source could be NADPH oxidase-like and superoxide dismutase activity, as has been shown for elicitor and salt-induced accumulation of ROS (Leshem et al, 2006;Ashtamker et al, 2007;Suzuki et al, 2011). Similarly, biotic elicitors are known to initiate ROS, likely through activation of calcium and phosphorylation cascades (Sagi and Fluhr, 2001;Fluhr, 2009;Dubiella et al, 2013).…”

Section: Discussionmentioning

confidence: 98%

Singlet Oxygen Signatures Are Detected Independent of Light or Chloroplasts in Response to Multiple Stresses

et al. 2014

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The production of singlet oxygen is typically associated with inefficient dissipation of photosynthetic energy or can arise from light reactions as a result of accumulation of chlorophyll precursors as observed in fluorescent (flu)-like mutants. Such photodynamic production of singlet oxygen is thought to be involved in stress signaling and programmed cell death. Here we show that transcriptomes of multiple stresses, whether from light or dark treatments, were correlated with the transcriptome of the flu mutant. A core gene set of 118 genes, common to singlet oxygen, biotic and abiotic stresses was defined and confirmed to be activated photodynamically by the photosensitizer Rose Bengal. In addition, induction of the core gene set by abiotic and biotic selected stresses was shown to occur in the dark and in nonphotosynthetic tissue. Furthermore, when subjected to various biotic and abiotic stresses in the dark, the singlet oxygen-specific probe Singlet Oxygen Sensor Green detected rapid production of singlet oxygen in the Arabidopsis (Arabidopsis thaliana) root. Subcellular localization of Singlet Oxygen Sensor Green fluorescence showed its accumulation in mitochondria, peroxisomes, and the nucleus, suggesting several compartments as the possible origins or targets for singlet oxygen. Collectively, the results show that singlet oxygen can be produced by multiple stress pathways and can emanate from compartments other than the chloroplast in a light-independent manner. The results imply that the role of singlet oxygen in plant stress regulation and response is more ubiquitous than previously thought.

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“…RBOHs are plasma membrane-located enzymes that produce superoxide in the apoplast (Ros Barceló, 1998;Suzuki et al, 2011;Kärkönen and Kuchitsu, 2015). Remarkably, five putative RBOH genes were significantly up-regulated in non-lignin-forming conditions but none in conditions of lignin formation ( Fig.…”

Section: Apoplastic H 2 O 2 Production and Signalingmentioning

confidence: 99%

“…Candidates include isoenzymes of apoplastic peroxidases that can form H 2 O 2 if there is a reductant present (Daudi et al, 2012); however, the native apoplastic reductant is unknown. Other candidates include plasma membrane-located RBOH enzymes (Ros Barceló, 1998;Suzuki et al, 2011;Kärkönen and Kuchitsu, 2015). RBOHs generate apoplastic superoxide that dismutates to H 2 O 2 either nonenzymatically in the acidic pH present in the cell wall or enzymatically via a superoxide dismutase (SOD)-catalyzed reaction (Karlsson et al, 2005).…”

Section: Apoplastic Ros Generationmentioning

confidence: 99%

A Key Role for Apoplastic H₂O₂ in Norway Spruce Phenolic Metabolism

et al. 2017

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Apoplastic events such as monolignol oxidation and lignin polymerization are difficult to study in intact trees. To investigate the role of apoplastic hydrogen peroxide (H 2 O 2 ) in gymnosperm phenolic metabolism, an extracellular lignin-forming cell culture of Norway spruce (Picea abies) was used as a research model. Scavenging of apoplastic H 2 O 2 by potassium iodide repressed lignin formation, in line with peroxidases activating monolignols for lignin polymerization. Time-course analyses coupled to candidate substrate-product pair network propagation revealed differential accumulation of low-molecular-weight phenolics, including (glycosylated) oligolignols, (glycosylated) flavonoids, and proanthocyanidins, in lignin-forming and H 2 O 2 -scavenging cultures and supported that monolignols are oxidatively coupled not only in the cell wall but also in the cytoplasm, where they are coupled to other monolignols and proanthocyanidins. Dilignol glycoconjugates with reduced structures were found in the culture medium, suggesting that cells are able to transport glycosylated dilignols to the apoplast. Transcriptomic analyses revealed that scavenging of apoplastic H 2 O 2 resulted in remodulation of the transcriptome, with reduced carbon flux into the shikimate pathway propagating down to monolignol biosynthesis. Aggregated coexpression network analysis identified candidate enzymes and transcription factors for monolignol oxidation and apoplastic H 2 O 2 production in addition to potential H 2 O 2 receptors. The results presented indicate that the redox state of the apoplast has a profound influence on cellular metabolism.

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Respiratory burst oxidases: the engines of ROS signaling

Cited by 867 publications

References 60 publications

Reactive Oxygen Species-Driven Transcription in Arabidopsis under Oxygen Deprivation

Reactive Oxygen Species-Driven Transcription in Arabidopsis under Oxygen Deprivation

Singlet Oxygen Signatures Are Detected Independent of Light or Chloroplasts in Response to Multiple Stresses

A Key Role for Apoplastic H₂O₂ in Norway Spruce Phenolic Metabolism

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Respiratory burst oxidases: the engines of ROS signaling

Cited by 867 publications

References 60 publications

Reactive Oxygen Species-Driven Transcription in Arabidopsis under Oxygen Deprivation

Reactive Oxygen Species-Driven Transcription in Arabidopsis under Oxygen Deprivation

Singlet Oxygen Signatures Are Detected Independent of Light or Chloroplasts in Response to Multiple Stresses

A Key Role for Apoplastic H2O2 in Norway Spruce Phenolic Metabolism

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A Key Role for Apoplastic H₂O₂ in Norway Spruce Phenolic Metabolism