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Intracellular pathway of catalase synthesis. Low, P. Decreases in total ascorbate are sometimes observed in cat2 , although these are relatively minor compared with the marked increase in total glutathione Queval et al. Total ascorbate pools in wild-type plants are highly influenced by growth irradiance Grace and Logan, ; Gatzek et al. In tobacco Cat1 knockdowns, increased H 2 O 2 stress was triggered by transferring plants from low to moderate light Willekens et al.
While this treatment caused ascorbate contents to increase 4-fold within 2 d in wild-type tobacco plants, no increase was observed in the catalase-deficient lines Willekens et al. Evidence that enhanced availability of intracellular H 2 O 2 opposes certain other responses to increased irradiance has been presented in studies of Arabidopsis CAT2 knockdowns Vandenabeele et al.
Electron flow between glutathione and ascorbate Fig. Enhanced activity of the ascorbate—glutathione pathway when catalase is deficient was evidenced by induction of APX and DHARs at both the transcript level and by enzyme activity Willekens et al. Changes at transcript level were specific to cytosolic forms of these enzymes in Arabidopsis cat2 and cat2 gr1 mutants Mhamdi et al.
This points to a close coupling of increased peroxisomal H 2 O 2 availability and cytosolic antioxidant systems, consistent with the demonstrated importance of cytosolic APX1 in Arabidopsis Davletova et al.
H 2 O 2 -triggered oxidation of glutathione in cat2 may also be mediated through ascorbate-independent pathways Fig. Catalase-deficient tobacco shifted to high light to induce photorespiration showed the accumulation of GPX proteins alongside APX Willekens et al. However, thioredoxins are more efficient reductants for annotated GPXs than glutathione Iqbal et al.
A more significant route for direct peroxidation of GSH could be through glutathione S -transferases GSTs , many of which have peroxidase activity Dixon et al. Several GSTs are strongly induced in catalase-deficient lines Vanderauwera et al. The effects of the gr1 mutation on the cat2 phenotype contrast intriguingly with the ameliorated phenotype observed when cytosolic APX activity is down-regulated in tobacco CAT1 knockdowns Rizhsky et al.
Interestingly, the ameliorated phenotype of Arabidopsis mutants that are deficient in both CAT2 and cytosolic APX is correlated with the induction of a network of DNA repair, cell cycle control, and ER cell death pathways Vanderauwera et al. This conclusion is consistent with the observed gene expression patterns. Further work is required to establish which glutathione-associated peroxidases are most important in ascorbate-independent reduction of H 2 O 2 or derived peroxides.
A major advantage of using C 3 plants deficient in Class I catalases to modify cell redox state is that the rate of intracellular H 2 O 2 production can be readily modulated by irradiance and switched off in the light by high CO 2. This feature enables redox state to be conditional and controllably perturbed. Growth of Arabidopsis cat2 at high CO 2 prevents redox perturbation and hence the marked phenotype observed during growth in air Fig.
Transferring cat2 back to air causes the onset of measurable oxidative stress within hours to days, as evidenced by changes in glutathione status Fig. However, within a time-scale of several days after transfer, little effect of the oxidative stress on the plant phenotype is observed. Thus, catalase-deficient plants allow early and late events in oxidative signalling pathways to be studied, within the overall aim of distinguishing between H 2 O 2 -dependent and -independent components involved in stress responses Fig.
Furthermore, the conditional photorespiratory nature of cat2 predicts that any effects of secondary mutations should be annulled by growth at high CO 2. For example, cat2 gr1 double mutants show a phenotype that is much more severe than cat2 grown in air.
However, when cat2 and cat2 gr1 are grown at high CO 2 , they display similar phenotypes to wild-type and gr1 single mutants Mhamdi et al. Conditional photorespiratory nature of cat2 and its application in the analysis of H 2 O 2 signalling processes. A Dependence of cat2 phenotype and leaf redox state on photorespiratory H 2 O 2 production. Specific conditions were 5 weeks in air left , 3 weeks at ppm CO 2 middle , or 3 weeks at high CO 2 and subsequently transferred for 4 d to air right.
Glutathione was assayed as a marker for leaf redox state in each condition. B Scheme showing the use of cat2 and similar plants to identify H 2 O 2 -specific signalling pathways likely to be important in stress conditions. Although stress conditions are perceived by the plant through H 2 O 2 -independent pathways which may be specific to a stress or common between different stresses , most stresses involve redox signalling mediated through components such as H 2 O 2.
The conditional nature of the catalase-deficient mutants enables H 2 O 2 -dependent signalling to be studied by varying intensity irradiance, CO 2 level and also duration kinetics studies after transfer from low to high light or from high CO 2 to air.
Two related but distinct questions arise from studies of catalase-deficient plants: i How relevant are effects observed in such systems to those occurring during stress? Considerable information on H 2 O 2 -induced changes in gene expression has been generated by studies of catalase-deficient tobacco and Arabidopsis lines Vandenabeele et al. Analysis of transcription factors that responded rapidly on shifting Arabidopsis CAT2 knockdowns to high light revealed that several were also affected by abiotic stresses such as cold, heat, and drought Vanderauwera et al.
Several of these H 2 O 2 -induced transcription factors are now established regulators of abiotic stress responses Shinozaki and Yamaguchi-Shinozaki, ; Davletova et al. Furthermore, many of the genes that were strongly induced in Arabidopsis cat2 knockouts after transfer from high CO 2 to air Queval et al. Furthermore, a complex pattern of different ROS-responsive genes has been identified during various abiotic stresses, suggesting that different abiotic stress conditions provoke the production of different ROS and that transcriptome profiling analyses could predict the degree of involvement of a specific ROS during a specific stress condition Gadjev et al.
Examples of genes that are conditionally induced in cat2 and a summary of their responses to environmental stresses or hormones. The selected genes represent those most strongly induced in the cat2 knockout mutant, based on transcriptomic footprinting of about Arabidopsis genes Queval et al.
The numbered stress conditions are as follows. Bacteria P. Fungi B. Salicylic acid. Abscisic acid. Methyl jasmonate. Phenotypes of tobacco and Arabidopsis lines suggest that catalase deficiency mimics biotic stress particularly strongly.
Under conditions favouring photorespiration, responses include lesion formation, accumulation of SA and induction of PR genes Chamnongpol et al. In Arabidopsis cat2 , the formation of lesions is daylength-dependent Fig. All these responses are absent when oxidative stress occurs under short-day conditions, even though the intracellular thiol-disulphide state is at least as perturbed in short days as in long days.
However, responses can be induced in short days by supplementation of exogenous SA and reverted in long days by extinction of SA synthesis through the isochorismate pathway Chaouch et al. Together, these observations show that cat2 grown in long-day conditions is a constitutive defence mutant in which peroxisomal H 2 O 2 triggers SA-dependent hypersensitive response HR -like lesion formation Chaouch et al.
While most of the focus on pathogen-associated ROS production has focused on apoplastic events Bindschedler et al. Key peroxisomal biogenesis genes are induced by stresses, including H 2 O 2 Lopez-Huertas et al. Indications of a role for photorespiratory H 2 O 2 in pathogen responses come from studies of plants with altered serine:glyoxylate aminotransferase activity Taler et al.
As discussed above, perturbation of glutathione is one of the clearest responses to increased H 2 O 2 availability. Environmental stresses also trigger qualitatively similar changes to those observed in catalase-deficient plants, i. Redox-sensitive in vivo probes revealed perturbation of glutathione redox state in Arabidopsis subjected to water stress Jubany-Mari et al.
Glutathione and related thiols are well known to be involved in pathogen responses, including induction of PR genes and phytoalexin synthesis Edwards et al. In Arabidopsis , the expression of some PR genes is under the control of the SA-dependent signalling component, NPR1, which is regulated by cytosolic thiol-disulphide components involving thioredoxins and, potentially, glutathione Tada et al.
Studies of SA responses in cat2 backgrounds suggest that catalase deficiency recapitulates at least some of the pathogen-related responses involving cytosolic NADP-dependent thiol-disulphide systems Chaouch et al. Thus, cat2 and similar systems are likely to be particularly useful in the evaluation of in vivo interactions between H 2 O 2 and thiol components.
As shown in Fig. The absence of an HR-like response in cat2 in short days is not linked to insufficient oxidative stress. Accumulation of both glutathione Fig. Recovery of lesion formation and a range of other pathogen responses in cat2 in short days by SA treatment suggests that either daylength or the duration rather than the intensity of oxidative stress governs a switch between H 2 O 2 responses that do not require SA accumulation in short days and SA-dependent HR-like programmes in long days Chaouch et al.
Such an interpretation is consistent with observations of other lesion-mimic mutants Dietrich et al. Links between phytochrome signalling and SA accumulation and between SA, flowering and defence reactions have been reported Genoud et al. Ozone-induced leaf damage was shown to be influenced by the photoperiod context in which plants were subjected to equal-time treatments Vollsnes et al. In both animals and plants, ROS have been implicated in ageing and catalase may play a role in senescence.
However, transgenic mice in which the single mammalian catalase gene is knocked out show normal development Ho et al. Knockout of peroxisomal catalase in C. In humans, catalase deficiency has recently been implicated in greying of hair Wood et al. In Arabidopsis , CAT2 expression decreases after flowering and this decrease has been proposed to be an integral part of H 2 O 2 -triggered leaf senescence Zimmerman et al.
However, the senescence marker SAG12 was not among the genes induced by catalase inhibition Navabpour et al. Genes induced by photorespiratory H 2 O 2 in cat2 include some that are induced during senescence Table 3. Despite this, the cat2 phenotypes do not provide strong evidence for a co-ordinated activation of senescence programmes by peroxisomal H 2 O 2 , and this view is supported by other data from transcriptomic profiling.
Experiments over a longer time-scale 2—4 d after transfer of cat2 knockouts from high CO 2 to air also show that WRKY53 is not significantly induced in response to increases in peroxisomal H 2 O 2 Mhamdi et al. The lesion phenotype and other responses of cat2 in long days are clearly more similar to HR-like processes than to senescence, while in short days cat2 plants have a decreased growth rather than altered senescence.
Furthermore, CAT3 transcripts are not increased in cat2 Queval et al. The growth restraint observed in cat2 possibly involves mechanisms common to many environmental stresses, reflecting the centrality of redox state in these conditions. The link between H 2 O 2 and senescence appears to be complex and future studies will further unravel the roles of catalase regulation in this process. Numerous studies of plant responses to various stresses have included data on changes in catalase activity or expression.
A detailed analysis of this literature is beyond the scope of the present review. The following discussion focuses on potential mechanisms by which regulation of catalase could contribute to oxidative signalling, with a particular focus on increases in H 2 O 2 availability that could result from down-regulation of catalase. A first mode of possible regulation is through changes in transcript abundance.
Potato Class II catalase was induced in roots exposed to nematodes and bacteria and by SA in stem tissue Niebel et al. Similar induction of Class II catalase was observed in tobacco leaves treated with tobacco mosaic virus or fungal elicitor Dorey et al. Intriguingly, in view of the observations in catalase-deficient plants, Class I catalase transcripts were down-regulated by these treatments Dorey et al.
This discrepancy may reflect the importance of developmental stage or the sub cellular localization of H 2 O 2 signals. CAT1 transcripts were also induced by abscisic acid through a pathway dependent on mitogen-activated protein kinase-dependent signalling Xing et al. However, as discussed above, phenotypic and other effects observed in cat2 knockouts do not point to a simple relationship between CAT2 expression and senescence.
A second potential mode of regulation of catalase activity is at the post-transcriptional level. Selective degradation of catalase was reported to be a trigger of autophagic cell death in animal cells Yu et al.
One well-described mechanism in plants is diminished re-synthesis of catalase in stress conditions. Catalase is a light-sensitive protein that has a high turnover rate, and stresses such as cold, salt, and high light can cause decreases in the total protein through accelerated inactivation or decreased capacity to replace the protein Volk and Feierabend, ; Hertwig et al. Re-synthesis of rye Cat1 is post-transcriptionally controlled by mRNA methylation, which is stimulated by blue light and peroxides Schmidt et al.
Other potential mechanisms that could down-regulate catalase activity include SA and nitric oxide Vlot et al. As noted above, it is also possible that ROS homeostasis is affected by catalase targeting efficiency and potential changes in subcellular distribution. In Chlamydomonas , which lack peroxisomes, mitochondrial catalase activity is inhibited by light via a redox-dependent mechanism involving chloroplast thioredoxins Shao et al. Several proteins have been identified that could interact with catalase polypeptides.
Calmodulin was shown to be present in peroxisomes and to increase the activity of tobacco catalase but not catalases from a bacterium, a fungus, or humans Yang and Poovaiah, Catalases have also been found to interact with nucleoside disphosphate kinase 1 NDK1 , a cytosolic protein Fukamatsu et al.
This interaction may also increase catalase activity Fukamatsu et al. Both associations could modulate the activity of any catalase that may be found in the cytosol. However, it remains unclear whether these interactions reflect in vivo phenomena because NDPK2, which was also found to interact with SOS2 Verslues et al.
It remains unclear whether natural genetic variability in catalase could contribute to differences in stress responses, though there is sufficient allelic variability at the maize Cat3 locus to encode electrophoretically distinguishable proteins Scandalios et al. A maize line showing increased resistance to Aspergillus flavus infection had a Cat3 allele with a deletion of 20 amino acids compared to the control line Magbanua et al.
Concepts of ROS as toxic compounds have been qualified over recent years by the realization that they are also important signal molecules. It is often considered that concentration is a key factor in determining which of these modes ROS operate through. However, observations that singlet oxygen-induced bleaching can be genetically reverted Wagner et al. It is therefore likely that ROS signalling is a more useful conceptual paradigm than damage, even when this involves marked intracellular redox perturbation that results from the loss of a highly active H 2 O 2 -metabolizing enzyme.
Further, analysis of biochemical markers of redox state in cat2 and cat2 gr1 mutants points to a rather specific perturbation of glutathione, suggesting that altered status of this key redox buffer may act as an important channel for H 2 O 2 -triggered signal transduction. To exploit processes in which ROS act through widespread damage, preferred strategies would be to minimize ROS accumulation or the probability of interaction with sensitive components Fig.
However, if the physiological effects of ROS work primarily through a more limited number of signalling mechanisms, other approaches could be feasible, such as the selection of gain-of-function or loss-of-function mutants Fig. Although there could be overlap and interdependence between the two approaches enhancing defence or adjustment of signalling , the choice of experimental strategies will inevitably be influenced by which concept is dominant.
Whichever view is favoured, it is not likely to be simple to achieve the desired modifications in plant performance without less attractive trade-off effects.
However, this objective will probably be aided by improved knowledge on how redox signalling interfaces and interacts with the network of signalling pathways through components such as phytohormones. The growing awareness of the crucial role of redox-dependent signalling in plant development and function suggests that conditional catalase-deficient mutants are likely to continue to be useful tools to this end.
Alternative models of oxidative stress-mediated effects and potential strategies to modulate them. Google Scholar. Google Preview. Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide. Sign In or Create an Account. Sign In. Advanced Search.
Search Menu. Article Navigation. Close mobile search navigation Article Navigation. Volume Article Contents Abstract. Stress and reactive oxygen.
Plant catalases. Genetic manipulation of catalase. Modification of cell redox state in catalase-deficient plants. Physiological significance of studies of catalase mutants. Conclusions and perspectives. Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. Amna Mhamdi , Amna Mhamdi. Oxford Academic. Guillaume Queval. Sejir Chaouch.
Sandy Vanderauwera. Frank Van Breusegem. Revision received:. Select Format Select format. Permissions Icon Permissions. Abstract Hydrogen peroxide H 2 O 2 is an important signal molecule involved in plant development and environmental responses. Arabidopsis thaliana , glutathione , H 2 O 2 , mutants , oxidative stress , pathogens , redox signalling. Open in new tab Download slide.
Table 1. Open in new tab. Table 2. Table 3. P, put. Narrowing the agronomic yield gap with improved nitrogen use efficiency: a modeling approach.
Google Scholar Crossref. Search ADS. Effects of inhibitors of catalase on photosynthesis and on catalase activity in unwashed preparations of intact chloroplasts. Enhanced tolerance to photooxidative stress of transgenic Nicotiana tabacum with high chloroplastic glutathione reductase activity.
The water—water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Arabidopsis mutants reveal multiple singlet oxygen signaling pathways involved in stress response and development. Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Inhibition of catalase activity is an early response of Arabidopsis thaliana cultured cells to the phytotoxin fusicoccin. Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance.
Manipulation of catalase levels produces altered photosynthesis in transgenic tobacco plants. Oxidative stress responses in transgenic tobacco containing altered levels of glutathione reductase activity.
The lithium tolerance of the Arabidopsis cat2 mutant reveals a cross-talk between oxidative stress and ethylene. Transgenic tobacco with a reduced catalase activity develops necrotic lesions and induces pathogenesis-related expression under high light. Defense activation and enhanced pathogen tolerance induced by H 2 O 2 in transgenic plants. Genetic reversion of cell death in the Arabidopsis cat2 knockout mutant shows that peroxisomal H 2 O 2 is coupled to biotic defense responses by isochorismate synthase 1 in a daylength-related manner.
Peroxisomal xanthine oxidoreductase: characterization of the enzyme from pea Pisum sativum L. Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco paradoxically causes increased oxidative stress.
Catalase-deficient tobacco plants: tools for in planta studies on the role of hydrogen peroxide. Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. Mechanism of the inhibition of catalase by ascorbate. Roles of active oxygen species, copper and semidehydroascorbate. Google Scholar PubMed.
Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis.
A more sensitive modification of the catalase assay with the Clark oxygen electrode: application to the kinetic study of the pea leaf enzyme. Reactive oxygen species and reactive nitrogen species in peroxisomes.
Production, scavenging, and role in cell signaling. Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. Tobacco class I and II catalases are differentially expressed during elicitor-induced hypersensitive cell death and localized acquired resistance. Role for salicylic acid in the activation of defense responses in catalase-deficient transgenic tobacco. Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity and determine stress resistance through altered signaling and diurnal regulation.
Glutathione and elicitation of the phytoalexin response in legume cell cultures. Generation of hydrogen peroxide in chloroplasts of Arabidopsis overexpressing glcyolate oxidase as an inducible system to study oxidative stress. Effect of 3-amino-1,2,4-triazole, a catalase inhibitor, on peroxide content of suspension-cultured pear fruit cells. Photorespiratory metabolism: genes, mutants, energetics, and redox signaling.
The presence of dehydroascorbate and dehydroascorbate reductase in plant tissues. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Overexpression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees.
Glutathione and homoglutathione play a critical role in the nodulation process of Medicago truncatula. Catalase is encoded by a multigene family in Arabidopsis thaliana L.
Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Antisense suppression of l -galactose dehydrogenase in Arabidopsis thaliana provides evidence for its role in ascorbate synthesis and reveals light-modulated l -galactose synthesis.
Phytochrome signalling modulates the SA—perceptive pathway in Arabidopsis. The intercellular distribution of glutathione synthesis and its response to chilling in maize. Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen species.
Molecular evolution of maize catalases and their relationship to other eukaryotic and prokaryotic catalases. Changes in H 2 O 2 availability can result from increased production or decreased metabolism. While plants contain several types of H 2 O 2 -metabolizing proteins, catalases are highly active enzymes that do not require cellular reductants as they primarily catalyse a dismutase reaction.
This review provides an update on plant catalase genes, function, and subcellular localization, with a focus on recent information generated from studies on Arabidopsis.
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