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Journal ArticleDOI

The Calcineurin B-Like Calcium Sensors CBL1 and CBL9 Together with Their Interacting Protein Kinase CIPK26 Regulate the Arabidopsis NADPH Oxidase RBOHF

TL;DR: A direct interconnection between CBL-CIPK-mediated Ca(2+) signaling and ROS signaling in plants is identified and evidence for a synergistic activation of the NADPH oxidase RBOHF is provided by directCa(2+)-binding to its EF-hands and Ca( 2+)-induced phosphorylation by CBL1/9-C IPK26 complexes.
About: This article is published in Molecular Plant.The article was published on 2013-03-01 and is currently open access. It has received 327 citations till now. The article focuses on the topics: NADPH oxidase & Signal transduction.
Citations
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Journal ArticleDOI
06 Oct 2016-Cell
TL;DR: Core stress-signaling pathways involve protein kinases related to the yeast SNF1 and mammalian AMPK, suggesting that stress signaling in plants evolved from energy sensing.

2,853 citations


Cites background from "The Calcineurin B-Like Calcium Sens..."

  • ...ABA-activated SnRK2s also phosphorylate the plasma-membrane NADPH oxidase RbohF, which when phosphorylated generates O2 in the apoplastic space....

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  • ...Phosphatidic acid contributes to ABA signaling by binding to and activating RbohD and RbohF (Zhang et al., 2009)....

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  • ...Furthermore, ABA-triggered calcium signal can activate the CBL1/9-CIPK26 module to cause phosphorylation of effector proteins such as RbohF (Drerup et al., 2013)....

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Journal ArticleDOI
TL;DR: ROS is beneficial to plants during abiotic stress enabling them to adjust their metabolism and mount a proper acclimation response, as long as cells maintain high enough energy reserves to detoxify ROS.
Abstract: Reactive oxygen species (ROS) play a key role in the acclimation process of plants to abiotic stress. They primarily function as signal transduction molecules that regulate different pathways during plant acclimation to stress, but are also toxic byproducts of stress metabolism. Because each subcellular compartment in plants contains its own set of ROS-producing and ROS-scavenging pathways, the steady-state level of ROS, as well as the redox state of each compartment, is different at any given time giving rise to a distinct signature of ROS levels at the different compartments of the cell. Here we review recent studies on the role of ROS in abiotic stress in plants, and propose that different abiotic stresses, such as drought, heat, salinity and high light, result in different ROS signatures that determine the specificity of the acclimation response and help tailor it to the exact stress the plant encounters. We further address the role of ROS in the acclimation of plants to stress combination as well as the role of ROS in mediating rapid systemic signaling during abiotic stress. We conclude that as long as cells maintain high enough energy reserves to detoxify ROS, ROS is beneficial to plants during abiotic stress enabling them to adjust their metabolism and mount a proper acclimation response.

1,462 citations


Cites background from "The Calcineurin B-Like Calcium Sens..."

  • ...…at the guard cells with the ROS wave (Mittler and Blumwald, 2015) resulted in the opening of ROS-regulated Ca2+ channels that in turn induced the activation of RBOH by CIPK26 (Drerup et al., 2013), resulting in further biosynthesis of ROS and generating a positive feedback loop for stomata closure....

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  • ...H2O2 generated by RBOH-SOD and/or arriving at the guard cells with the ROS wave (Mittler and Blumwald, 2015) resulted in the opening of ROS-regulated Ca2+ channels that in turn induced the activation of RBOH by CIPK26 (Drerup et al., 2013), resulting in further biosynthesis of ROS and generating a positive feedback loop for stomata closure....

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Journal ArticleDOI
TL;DR: This review will provide an update of recent findings related to the integration of ROS signals with an array of signalling pathways aimed at regulating different responses in plants and address signals that confer systemic acquired resistance (SAR) or systemic acquired acclimation (SAA) in plants.
Abstract: Reactive oxygen species (ROS) play an integral role as signalling molecules in the regulation of numerous biological processes such as growth, development, and responses to biotic and/or abiotic stimuli in plants. To some extent, various functions of ROS signalling are attributed to differences in the regulatory mechanisms of respiratory burst oxidase homologues (RBOHs) that are involved in a multitude of different signal transduction pathways activated in assorted tissue and cell types under fluctuating environmental conditions. Recent findings revealed that stress responses in plants are mediated by a temporal-spatial coordination between ROS and other signals that rely on production of stress-specific chemicals, compounds, and hormones. In this review we will provide an update of recent findings related to the integration of ROS signals with an array of signalling pathways aimed at regulating different responses in plants. In particular, we will address signals that confer systemic acquired resistance (SAR) or systemic acquired acclimation (SAA) in plants.

1,414 citations


Cites background from "The Calcineurin B-Like Calcium Sens..."

  • ...In addition, a recent finding demonstrated that the activity of RBOHF is regulated by direct Ca 2+ binding to its EF-hands and Ca 2+ -dependent phosphorylation by CBL1/9–CIPK26 complexes (Drerup et al., 2013)....

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  • ...…depend on various signalling components including protein phosphorylation , Ca 2+ , calcium-dependent protein kinases (CDPKs), and phospholipase Dα1 (PLDα1) (Lin et al., 2009; Monshausen et al., 2009; Zhang et al., 2009; Jakubowicz et al., 2010; Drerup et al., 2013; Dubiella et al., 2013)....

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  • ...Unlike the mammalian counterpart , plant RBOHs have a cytosolic N-terminal extension comprised of two Ca 2+ -binding EF-hand motifs and phosphorylation target sites that are important for their activity (Kobayashi et al., 2007; Oda et al., 2010; Kimura et al., 2012; Drerup et al., 2013)....

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  • ...(B) Binding of Ca 2+ to EF-hand motifs is required for activation of RBOHs (Ogasawara et al., 2008; Drerup et al., 2013)....

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  • ...ABA is involved in a broad range of biological functions, and its integration with ROS has been revealed (Kwak et al., 2003; Sagi et al., 2004; Ma et al., 2012; Drerup et al., 2013)....

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Journal ArticleDOI
TL;DR: This study reveals a rapid regulatory mechanism of a plant RBOH, which occurs in parallel with and is essential for its paradigmatic calcium-based regulation.

687 citations


Cites background from "The Calcineurin B-Like Calcium Sens..."

  • ...In addition, Ca2+ activates Ca2+-regulated protein kinases, such as CPKs or calcineurin-B-like proteininteracting protein kinases (CIPKs), which can phosphorylate RBOHs (Boudsocq and Sheen, 2013; Gao et al., 2013; Dubiella et al., 2013; Kimura et al., 2013; Drerup et al., 2013)....

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Journal ArticleDOI
TL;DR: H2 O2 oxidizes specific cysteine residues of target proteins to the sulfenic acid form and, similar to other organisms, this modification could initiate thiol-based redox relays and modify target enzymes, receptor kinases and transcription factors.
Abstract: Contents Summary 1197 I Introduction 1198 II Measurement and imaging of H2 O2 1198 III H2 O2 and O2 ·- toxicity 1199 IV Production of H2 O2 : enzymes and subcellular locations 1200 V H2 O2 transport 1205 VI Control of H2 O2 concentration: how and where? 1205 VII Metabolic functions of H2 O2 1207 VIII H2 O2 signalling 1207 IX Where next? 1209 Acknowledgements 1209 References 1209 SUMMARY: Hydrogen peroxide (H2 O2 ) is produced, via superoxide and superoxide dismutase, by electron transport in chloroplasts and mitochondria, plasma membrane NADPH oxidases, peroxisomal oxidases, type III peroxidases and other apoplastic oxidases Intracellular transport is facilitated by aquaporins and H2 O2 is removed by catalase, peroxiredoxin, glutathione peroxidase-like enzymes and ascorbate peroxidase, all of which have cell compartment-specific isoforms Apoplastic H2 O2 influences cell expansion, development and defence by its involvement in type III peroxidase-mediated polymer cross-linking, lignification and, possibly, cell expansion via H2 O2 -derived hydroxyl radicals Excess H2 O2 triggers chloroplast and peroxisome autophagy and programmed cell death The role of H2 O2 in signalling, for example during acclimation to stress and pathogen defence, has received much attention, but the signal transduction mechanisms are poorly defined H2 O2 oxidizes specific cysteine residues of target proteins to the sulfenic acid form and, similar to other organisms, this modification could initiate thiol-based redox relays and modify target enzymes, receptor kinases and transcription factors Quantification of the sources and sinks of H2 O2 is being improved by the spatial and temporal resolution of genetically encoded H2 O2 sensors, such as HyPer and roGFP2-Orp1 These H2 O2 sensors, combined with the detection of specific proteins modified by H2 O2 , will allow a deeper understanding of its signalling roles

478 citations


Additional excerpts

  • ...Drerup et al. (2013) OST1/SnRK2....

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References
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Journal ArticleDOI
01 Dec 1996-Genetics
TL;DR: A novel multienzyme approach was used to generate a set of highly representative genomic libraries from S. cerevisiae and a unique host strain was created that contains three easily assayed reporter genes, each under the control of a different inducible promoter.
Abstract: The two-hybrid system is a powerful technique for detecting protein-protein interactions that utilizes the well-developed molecular genetics of the yeast Saccharomyces cerevisiae. However, the full potential of this technique has not been realized due to limitations imposed by the components available for use in the system. These limitations include unwieldy plasmid vectors, incomplete or poorly designed two-hybrid libraries, and host strains that result in the selection of large numbers of false positives. We have used a novel multienzyme approach to generate a set of highly representative genomic libraries from S. cerevisiae. In addition, a unique host strain was created that contains three easily assayed reporter genes, each under the control of a different inducible promoter. This host strain is extremely sensitive to weak interactions and eliminates nearly all false positives using simple plate assays. Improved vectors were also constructed that simplify the construction of the gene fusions necessary for the two-hybrid system. Our analysis indicates that the libraries and host strain provide significant improvements in both the number of interacting clones identified and the efficiency of two-hybrid selections.

2,705 citations

Journal ArticleDOI
TL;DR: This review will attempt to address several key questions related to the use of ROS as signaling molecules in cells, including the dynamics and specificity of ROS signaling, networking of ROS with other signaling pathways, ROS signaling within and across different cells, ROS waves and the evolution of the ROS gene network.

1,879 citations

Journal ArticleDOI
TL;DR: Identification of two partially redundant Arabidopsis guard cell‐expressed NADPH oxidase catalytic subunit genes, AtrbohD and atrbohF, are reported, providing direct molecular genetic and cell biological evidence that ROS are rate‐limiting second messengers in ABA signaling, and that the AtrbOHD and AtrabohF NADPH oxidationases function in guard cell ABA signal transduction.
Abstract: Reactive oxygen species (ROS) have been proposed to function as second messengers in abscisic acid (ABA) signaling in guard cells. However, the question whether ROS production is indeed required for ABA signal transduction in vivo has not yet been addressed, and the molecular mechanisms mediating ROS production during ABA signaling remain unknown. Here, we report identification of two partially redundant Arabidopsis guard cell-expressed NADPH oxidase catalytic subunit genes, AtrbohD and AtrbohF, in which gene disruption impairs ABA signaling. atrbohD/F double mutations impair ABA-induced stomatal closing, ABA promotion of ROS production, ABA-induced cytosolic Ca2+ increases and ABA- activation of plasma membrane Ca2+-permeable channels in guard cells. Exogenous H2O2 rescues both Ca2+ channel activation and stomatal closing in atrbohD/F. ABA inhibition of seed germination and root elongation are impaired in atrbohD/F, suggesting more general roles for ROS and NADPH oxidases in ABA signaling. These data provide direct molecular genetic and cell biological evidence that ROS are rate-limiting second messengers in ABA signaling, and that the AtrbohD and AtrbohF NADPH oxidases function in guard cell ABA signal transduction.

1,555 citations

Journal ArticleDOI
TL;DR: The implementation of a bimolecular fluorescence complementation technique for visualization of protein-protein interactions in plant cells revealed a remarkable signal fluorescence intensity of interacting protein complexes as well as a high reproducibility and technical simplicity of the method in different plant systems.
Abstract: Dynamic networks of protein-protein interactions regulate numerous cellular processes and determine the ability to respond appropriately to environmental stimuli. However, the investigation of protein complex formation in living plant cells by methods such as fluorescence resonance energy transfer has remained experimentally difficult, time consuming and requires sophisticated technical equipment. Here, we report the implementation of a bimolecular fluorescence complementation (BiFC) technique for visualization of protein-protein interactions in plant cells. This approach relies on the formation of a fluorescent complex by two non-fluorescent fragments of the yellow fluorescent protein brought together by association of interacting proteins fused to these fragments (Hu et al., 2002). To enable BiFC analyses in plant cells, we generated different complementary sets of expression vectors, which enable protein interaction studies in transiently or stably transformed cells. These vectors were used to investigate and visualize homodimerization of the basic leucine zipper (bZIP) transcription factor bZIP63 and the zinc finger protein lesion simulating disease 1 (LSD1) from Arabidopsis as well as the dimer formation of the tobacco 14-3-3 protein T14-3c. The interaction analyses of these model proteins established the feasibility of BiFC analyses for efficient visualization of structurally distinct proteins in different cellular compartments. Our investigations revealed a remarkable signal fluorescence intensity of interacting protein complexes as well as a high reproducibility and technical simplicity of the method in different plant systems. Consequently, the BiFC approach should significantly facilitate the visualization of the subcellular sites of protein interactions under conditions that closely reflect the normal physiological environment.

1,498 citations

Journal ArticleDOI
TL;DR: In this paper, the authors analyzed lines carrying dSpm insertions in the highly expressed AtrbohD and AtrabohF genes, which are required for full ROI production observed during incompatible interactions with the bacterial pathogen Pseudomonas syringae pv.
Abstract: Reactive oxygen intermediates (ROI) are strongly associated with plant defense responses. The origin of these ROI has been controversial. Arabidopsis respiratory burst oxidase homologues (rboh genes) have been proposed to play a role in ROI generation. We analyzed lines carrying dSpm insertions in the highly expressed AtrbohD and AtrbohF genes. Both are required for full ROI production observed during incompatible interactions with the bacterial pathogen Pseudomonas syringae pv. tomato DC3000(avrRpm1) and the oomycete parasite Peronospora parasitica. We also observed reduced cell death, visualized by trypan blue stain and reduced electrolyte leakage, in the Atrboh mutants after DC3000(avrRpm1) inoculation. However, enhanced cell death is observed after infection of mutant lines with P. parasitica. Paradoxically, although atrbohD mutation eliminated the majority of total ROI production, atrbohF mutation exhibited the strongest effect on cell death.

1,491 citations