Plant cysteine oxidases control the oxygen-dependent branch of the N-end-rule pathway

Weits, Daan A.; Giuntoli, Beatrice; Kosmacz, Monika; Parlanti, Sandro; Hubberten, Hans Michael; Riegler, Heike; Hoefgen, Rainer; Perata, Pierdomenico; Dongen, Joost T. van; Licausi, Francesco

doi:10.1038/ncomms4425

Cited by 294 publications

(349 citation statements)

References 35 publications

(60 reference statements)

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“…These enzymes introduce two oxygen groups into an Nterminal thiol to produce cysteine sulfinic acid groups, a reaction that promotes protein degradation in the oxygen-dependent branch of the N-end rule pathway of targeted proteolysis (17) In the N-end rule pathway, the removal of the relatively stabilizing Nterminal methionine in certain transcription factors reveals a cysteine residue that is sensitive to S-nitrosylation as well as oxidation to sulfenic and sulfonic acid groups (18).…”

Section: Gsh and Redox Signallingmentioning

confidence: 99%

Glutathione – linking cell proliferation to oxidative stress

Díaz‐Vivancos

Simone

Kiddle³

et al. 2015

Free Radical Biology and Medicine

261

164

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Significance:The multifaceted functions of reduced glutathione (gamma-glutamyl-cysteinyl-glycine; GSH) continue to fascinate plants and animal scientists, not least because of the dynamic relationships between GSH and reactive oxygen species (ROS) that underpin reduction/oxidation (redox) regulation and signalling. Here we consider the respective roles of ROS and GSH in the regulation of plant growth, with a particular focus on regulation of the plant cell cycle. Glutathione is discussed not only as a crucial low molecular weight redox buffer that shields nuclear processes against oxidative challenge but also a flexible regulator of genetic and epigenetic functions. Recent Advances:The intracellular compartmentalization of GSH during the cell cycle is remarkably consistent in plants and animals. Moreover, measurements of in vivo glutathione redox potentials reveal that the cellular environment is much more reducing than predicted from GSH/GSSG ratios measured in tissue extracts. The redox potential of the cytosol and nuclei of non-dividing plant cells is about -300 mV. This relatively low redox potential is maintained even in cells experiencing oxidative stress by a number of mechanisms including vacuolar sequestration of GSSG. We propose that regulated ROS production linked to glutathione-mediated signalling events are the hallmark of viable cells within a changing and challenging environment. Critical Issues:The concept that the cell cycle in animals is subject to redox controls is well established but little is known about how ROS and GSH regulate this process in plants. However, it is increasingly likely that similar redox controls exist in plants, 3 although possibly through different pathways. Moreover, redox-regulated proteins that function in cell cycle checkpoints remain to be identified in plants. While GSHresponsive genes have now been identified, the mechanisms that mediate and regulate protein glutathionylation in plants remain poorly defined.Future Directions: The nuclear GSH pool provides an appropriate redox environment for essential nuclear functions. Future work will function on how this essential thiol interacts with the nuclear thioredoxin system and nitric oxide to regulate genetic and epigenetic mechanisms. The characterization of redox-regulated cell cycle proteins in plants, and the elucidation of mechanisms that facilitate GSH accumulation in the nucleus are keep steps to unravelling the complexities of nuclear redox controls.Diaz 4

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Section: Gsh and Redox Signallingmentioning

confidence: 99%

Glutathione – linking cell proliferation to oxidative stress

Díaz‐Vivancos

Simone

Kiddle³

et al. 2015

Free Radical Biology and Medicine

261

164

View full text Add to dashboard Cite

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“…The quintuple erfVII mutant (Marín-de la ) is a null mutant for RAP2.2, RAP2.3, RAP2.12, HRE1, HRE2, and a knockdown for RAP2.2 (Giuntoli et al, 2017b); a line constitutively expressing a version of the RAP2.12 protein that is also stable in air (35S:D-RAP2.12; Licausi et al, 2011); a line expressing GUS under the control of the PCO1 promoter (pPCO1:GUS; Weits et al, 2014); and a line overexpressing HRA1 . The bzip63 mutant and the bZIP63 overexpressor (35S:bZIP63) (Mair et al, 2015), two independent KIN10 overexpressor lines (OE1 KIN10 and OE2 KIN10) (Baena-González et al, 2007); the Arabidopsis SnRK1.1 dominant-negative mutant (SnRK1.1 K48M ; Cho et al, 2016); a line expressing RAP2.3 with an HA tag (35S:RAP2.3-HA; Gibbs et al, 2014).…”

Section: Plant Materialsmentioning

confidence: 99%

Gene Regulation and Survival under Hypoxia Requires Starch Availability and Metabolism

et al. 2017

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Plants respond to hypoxia, often caused by submergence, by expressing a specific set of genes that contribute to acclimation to this unfavorable environmental condition. Genes induced by low oxygen include those encoding enzymes for carbohydrate metabolism and fermentation, pathways that are required for survival. Sugar availability is therefore of crucial importance for energy production under hypoxia. Here, we show that Arabidopsis (Arabidopsis thaliana) plants require starch for surviving submergence as well as for ensuring the rapid induction of genes encoding enzymes required for anaerobic metabolism. The starchless pgm mutant is highly susceptible to submergence and also fails to induce anaerobic genes at the level of the wild type. Treating wild-type plants under conditions inducing sugar starvation results in a weak induction of alcohol dehydrogenase and other anaerobic genes. Induction of gene expression under hypoxia requires transcription factors belonging to group VII ethylene response factors (ERF-VII) that, together with plant Cys oxidases, act as an oxygen-sensing mechanism. We show that repression of this pathway by sugar starvation occurs downstream of the hypoxia-dependent stabilization of ERF-VII proteins and independently of the energy sensor protein kinases SnRK1

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“…The presence of molecular oxygen leads to oxidation of the penultimate Cys in the N terminus of RAP2.12 by specific plant Cys oxidases, targeting RAP2.12 to proteasomal degradation and leading to its destabilization (Weits et al, 2014). This is prevented in Arabidopsis plants overexpressing D13RAP2.12, which lacks the first 13 amino acids from the N terminus including the regulatory Cys and representing an N-end-rule-insensitive version of RAP2.12 (Licausi et al, 2011c).…”

mentioning

confidence: 99%

Oxygen Sensing via the Ethylene Response Transcription Factor RAP2.12 Affects Plant Metabolism and Performance under Both Normoxia and Hypoxia

et al. 2016

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Subgroup-VII-ethylene-response-factor (ERF-VII) transcription factors are involved in the regulation of hypoxic gene expression and regulated by proteasome-mediated proteolysis via the oxygen-dependent branch of the N-end-rule pathway. While research into ERF-VII mainly focused on their role to regulate anoxic gene expression, little is known on the impact of this oxygen-sensing system in regulating plant metabolism and growth. By comparing Arabidopsis (Arabidopsis thaliana) plants overexpressing N-end-rule-sensitive and insensitive forms of the ERF-VII-factor RAP2.12, we provide evidence that oxygen-dependent RAP2.12 stability regulates central metabolic processes to sustain growth, development, and anoxic resistance of plants. (1) Under normoxia, overexpression of N-end-rule-insensitive D13RAP2.12 led to increased activities of fermentative enzymes and increased accumulation of fermentation products, which were accompanied by decreased adenylate energy states and starch levels, and impaired plant growth and development, indicating a role of oxygen-regulated RAP2.12 degradation to prevent aerobic fermentation. (2) In D13RAP2.12-overexpressing plants, decreased carbohydrate reserves also led to a decrease in anoxic resistance, which was prevented by external Suc supply. (3) Overexpression of D13RAP2.12 led to decreased respiration rates, changes in the levels of tricarboxylic acid cycle intermediates, and accumulation of a large number of amino acids, including Ala and g-amino butyric acid, indicating a role of oxygen-regulated RAP2.12 abundance in controlling the flux-modus of the tricarboxylic acid cycle. (4) The increase in amino acids was accompanied by increased levels of immune-regulatory metabolites. These results show that oxygen-sensing, mediating RAP2.12 degradation is indispensable to optimize metabolic performance, plant growth, and development under both normoxic and hypoxic conditions.

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Plant cysteine oxidases control the oxygen-dependent branch of the N-end-rule pathway

Cited by 294 publications

References 35 publications

Glutathione – linking cell proliferation to oxidative stress

Glutathione – linking cell proliferation to oxidative stress

Gene Regulation and Survival under Hypoxia Requires Starch Availability and Metabolism

Oxygen Sensing via the Ethylene Response Transcription Factor RAP2.12 Affects Plant Metabolism and Performance under Both Normoxia and Hypoxia

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