The Involvement of Cysteine Proteases and Protease Inhibitor Genes in the Regulation of Programmed Cell Death in Plants

doi:10.1105/TPC.11.3.431

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The Involvement of Cysteine Proteases and Protease Inhibitor Genes in the Regulation of Programmed Cell Death in Plants

Journal Article•DOI•

The Involvement of Cysteine Proteases and Protease Inhibitor Genes in the Regulation of Programmed Cell Death in Plants

Mazal Solomon¹, Beatrice Belenghi¹, Massimo Delledonne², Ester Menachem¹, Alex Levine¹ - Show less +1 more•Institutions (2)

Hebrew University of Jerusalem¹, Catholic University of the Sacred Heart²

01 Mar 1999-The Plant Cell (American Society of Plant Biologists)-Vol. 11, Iss: 3, pp 431-443

TL;DR: It is shown that in soybean cells, PCD-activating oxidative stress induced a set of cysteine proteases, and a new role for proteinase inhibitor genes as modulators of PCD in plants is proposed.

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Abstract: Programmed cell death (PCD) is a process by which cells in many organisms die. The basic morphological and biochemical features of PCD are conserved between the animal and plant kingdoms. Cysteine proteases have emerged as key enzymes in the regulation of animal PCD. Here, we show that in soybean cells, PCD-activating oxidative stress induced a set of cysteine proteases. The activation of one or more of the cysteine proteases was instrumental in the PCD of soybean cells. Inhibition of the cysteine proteases by ectopic expression of cystatin, an endogenous cysteine protease inhibitor gene, inhibited induced cysteine protease activity and blocked PCD triggered either by an avirulent strain of Pseudomonas syringae pv glycinea or directly by oxidative stress. Similar expression of serine protease inhibitors was ineffective. A glutathione S -transferase–cystatin fusion protein was used to purify and characterize the induced proteases. Taken together, our results suggest that plant PCD can be regulated by activity poised between the cysteine proteases and the cysteine protease inhibitors. We also propose a new role for proteinase inhibitor genes as modulators of PCD in plants.

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Journal Article•DOI•

REACTIVE OXYGEN SPECIES: Metabolism, Oxidative Stress, and Signal Transduction

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Klaus Apel¹, Heribert Hirt²•Institutions (2)

École Polytechnique Fédérale de Lausanne¹, University of Vienna²

29 Apr 2004-Annual Review of Plant Biology

TL;DR: The mechanisms of ROS generation and removal in plants during development and under biotic and abiotic stress conditions are described and the possible functions and mechanisms for ROS sensing and signaling in plants are compared with those in animals and yeast.

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Abstract: Several reactive oxygen species (ROS) are continuously produced in plants as byproducts of aerobic metabolism. Depending on the nature of the ROS species, some are highly toxic and rapidly detoxified by various cellular enzymatic and nonenzymatic mechanisms. Whereas plants are surfeited with mechanisms to combat increased ROS levels during abiotic stress conditions, in other circumstances plants appear to purposefully generate ROS as signaling molecules to control various processes including pathogen defense, programmed cell death, and stomatal behavior. This review describes the mechanisms of ROS generation and removal in plants during development and under biotic and abiotic stress conditions. New insights into the complexity and roles that ROS play in plants have come from genetic analyses of ROS detoxifying and signaling mutants. Considering recent ROS-induced genome-wide expression analyses, the possible functions and mechanisms for ROS sensing and signaling in plants are compared with those in animals and yeast.

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9,908 citations

Cites background from "The Involvement of Cysteine Proteas..."

...Although the oxidative burst is a primary response to pathogen challenge that leads to PCD (15), and H 2O2 induces PCD in various systems (34, 70, 112),...
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...Studies show that a threshold exposure time of cells to H 2O2 is required, during which period transcription and translation are necessary (34, 112)....
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Journal Article•DOI•

Coordinated plant defense responses in Arabidopsis revealed by microarray analysis

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Peer M. Schenk¹, Kemal Kazan², Kemal Kazan¹, Iain W. Wilson³, Jonathan P. Anderson¹, Todd Richmond³, Shauna Somerville³, John M. Manners², John M. Manners¹ - Show less +5 more•Institutions (3)

University of Queensland¹, Commonwealth Scientific and Industrial Research Organisation², Carnegie Institution for Science³

10 Oct 2000-Proceedings of the National Academy of Sciences of the United States of America

TL;DR: The results indicated the existence of a substantial network of regulatory interactions and coordination occurring during plant defense among the different defense signaling pathways, notably between the salicylate and jasmonate pathways that were previously thought to act in an antagonistic fashion.

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Abstract: Disease resistance is associated with a plant defense response that involves an integrated set of signal transduction pathways. Changes in the expression patterns of 2,375 selected genes were examined simultaneously by cDNA microarray analysis in Arabidopsis thaliana after inoculation with an incompatible fungal pathogen Alternaria brassicicola or treatment with the defense-related signaling molecules salicylic acid (SA), methyl jasmonate (MJ), or ethylene. Substantial changes (up- and down-regulation) in the steady-state abundance of 705 mRNAs were observed in response to one or more of the treatments, including known and putative defense-related genes and 106 genes with no previously described function or homology. In leaf tissue inoculated with A. brassicicola, the abundance of 168 mRNAs was increased more than 2.5-fold, whereas that of 39 mRNAs was reduced. Similarly, the abundance of 192, 221, and 55 mRNAs was highly (>2.5-fold) increased after treatment with SA, MJ, and ethylene, respectively. Data analysis revealed a surprising level of coordinated defense responses, including 169 mRNAs regulated by multiple treatments/defense pathways. The largest number of genes coinduced (one of four induced genes) and corepressed was found after treatments with SA and MJ. In addition, 50% of the genes induced by ethylene treatment were also induced by MJ treatment. These results indicated the existence of a substantial network of regulatory interactions and coordination occurring during plant defense among the different defense signaling pathways, notably between the salicylate and jasmonate pathways that were previously thought to act in an antagonistic fashion.

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1,472 citations

Journal Article•DOI•

Hydrogen peroxide and nitric oxide as signalling molecules in plants

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Steven J. Neill¹, Radhika Desikan, Andrew Clarke, Roger D. Hurst, John T. Hancock - Show less +1 more•Institutions (1)

University of the West of England¹

15 May 2002-Journal of Experimental Botany

TL;DR: The potential roles of H( 2)O(2) and NO during various stresses and the signalling pathways they activate are discussed and key signalling components that might provide targets for enhancing crop production are identified.

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Abstract: It is now clear that hydrogen peroxide (H(2)O(2)) and nitric oxide (NO) function as signalling molecules in plants. A wide range of abiotic and biotic stresses results in H(2)O(2) generation, from a variety of sources. H(2)O(2) is removed from cells via a number of antioxidant mechanisms, both enzymatic and non-enzymatic. Both biotic and abiotic stresses can induce NO synthesis, but the biosynthetic origins of NO in plants have not yet been resolved. Cellular responses to H(2)O(2) and NO are complex, with considerable cross-talk between responses to several stimuli. In this review the potential roles of H(2)O(2) and NO during various stresses and the signalling pathways they activate are discussed. Key signalling components that might provide targets for enhancing crop production are also identified.

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1,199 citations

Cites background from "The Involvement of Cysteine Proteas..."

...PCD induced by H2O2 during the HR in Arabidopsis (Desikan et al., 1998a) and soybean (Solomon et al., 1999) requires transcription and translation, and several studies have demonstrated that H2O2 modulates gene expression during defence responses....
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..., 1998a) and soybean (Solomon et al., 1999) requires transcription and translation, and several studies have demonstrated that H2O2 modulates gene expression during defence responses....
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Journal Article•DOI•

Regulation of the Arabidopsis Transcriptome by Oxidative Stress

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Radhika Desikan¹, Soheila A.-H. Mackerness², John T. Hancock¹, Steven J. Neill¹•Institutions (2)

University of the West of England¹, University of Warwick²

01 Sep 2001-Plant Physiology

TL;DR: A large-scale analysis of the Arabidopsis transcriptome during oxidative stress identified 175 non-redundant expressed sequence tags that are regulated by H(2)O(2), and a substantial proportion have predicted functions in cell rescue and defense processes.

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Abstract: Oxidative stress, resulting from an imbalance in the accumulation and removal of reactive oxygen species such as hydrogen peroxide (H2O2), is a challenge faced by all aerobic organisms In plants, exposure to various abiotic and biotic stresses results in accumulation of H2O2 and oxidative stress Increasing evidence indicates that H2O2 functions as a stress signal in plants, mediating adaptive responses to various stresses To analyze cellular responses to H2O2, we have undertaken a large-scale analysis of the Arabidopsis transcriptome during oxidative stress Using cDNA microarray technology, we identified 175 non-redundant expressed sequence tags that are regulated by H2O2 Of these, 113 are induced and 62 are repressed by H2O2 A substantial proportion of these expressed sequence tags have predicted functions in cell rescue and defense processes RNA-blot analyses of selected genes were used to verify the microarray data and extend them to demonstrate that other stresses such as wilting, UV irradiation, and elicitor challenge also induce the expression of many of these genes, both independently of, and, in some cases, via H2O2

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918 citations

Cites background from "The Involvement of Cysteine Proteas..."

...Furthermore, several studies indicate that H2O2 is a key factor mediating programmed cell death (PCD) in response to pathogens, elicitors, and hormones (Tenhaken et al., 1995; Levine et al., 1996; Desikan et al., 1998a; Mittler et al., 1999; Solomon et al., 1999; Bethke and Jones, 2001)....
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...H2O2 induces PCD in Arabidopsis and other species (Levine et al., 1994; Desikan et al., 1998a; Mittler et al., 1999; Solomon et al., 1999); consequently, the expression of potential PCD-related genes following H2O2 treatment might be expected....
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Journal Article•DOI•

Programmed cell death, mitochondria and the plant hypersensitive response

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Eric Lam¹, Naohiro Kato¹, Michael T. Lawton¹•Institutions (1)

Rutgers University¹

14 Jun 2001-Nature

TL;DR: Many of the cell-death regulators that have been characterized in humans, worms and flies are absent from the Arabidopsis genome, indicating that plants probably use other regulators to control this process.

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Abstract: The plant response to attempted infection by microbial pathogens is often accompanied by rapid cell death in and around the initial infection site, a reaction known as the hypersensitive response. This response is associated with restricted pathogen growth and represents a form of programmed cell death (PCD). Recent pharmacological and molecular studies have provided functional evidence for the conservation of some of the basic regulatory mechanisms underlying the response to pathogens and the activation of PCD in animal and plant systems. In animals, the mitochondrion integrates diverse cellular stress signals and initiates the death execution pathway, and studies indicate a similar involvement for mitochondria in regulating PCD in plants. But many of the cell-death regulators that have been characterized in humans, worms and flies are absent from the Arabidopsis genome, indicating that plants probably use other regulators to control this process.

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875 citations

Cites background from "The Involvement of Cysteine Proteas..."

...For HR cell death in plants, cystatin-sensitive proteases have been found to be critical regulators in a soybean model syste...
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References

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Journal Article•DOI•

Caspases: the executioners of apoptosis

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Gerald M. Cohen¹•Institutions (1)

University of Leicester¹

15 Aug 1997-Biochemical Journal

TL;DR: The importance of caspase prodomains in the regulation of apoptosis is further highlighted by the recognition of adapter molecules, such as RAIDD [receptor-interacting protein (RIP)-associated ICH-1/CED-3-homologous protein with a death domain]/CRADD (caspase and RIP adapter with death domain), which binds to the prodomain of cspase-2 and recruits it to the signalling complex.

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Abstract: Apoptosis is a major form of cell death, characterized initially by a series of stereotypic morphological changes. In the nematode Caenorhabditis elegans, the gene ced-3 encodes a protein required for developmental cell death. Since the recognition that CED-3 has sequence identity with the mammalian cysteine protease interleukin-1 beta-converting enzyme (ICE), a family of at least 10 related cysteine proteases has been identified. These proteins are characterized by almost absolute specificity for aspartic acid in the P1 position. All the caspases (ICE-like proteases) contain a conserved QACXG (where X is R, Q or G) pentapeptide active-site motif. Capases are synthesized as inactive proenzymes comprising an N-terminal peptide (prodomain) together with one large and one small subunit. The crystal structures of both caspase-1 and caspase-3 show that the active enzyme is a heterotetramer, containing two small and two large subunits. Activation of caspases during apoptosis results in the cleavage of critical cellular substrates, including poly(ADP-ribose) polymerase and lamins, so precipitating the dramatic morphological changes of apoptosis. Apoptosis induced by CD95 (Fas/APO-1) and tumour necrosis factor activates caspase-8 (MACH/FLICE/Mch5), which contains an N-terminus with FADD (Fas-associating protein with death domain)-like death effector domains, so providing a direct link between cell death receptors and the caspases. The importance of caspase prodomains in the regulation of apoptosis is further highlighted by the recognition of adapter molecules, such as RAIDD [receptor-interacting protein (RIP)-associated ICH-1/CED-3-homologous protein with a death domain]/CRADD (caspase and RIP adapter with death domain), which binds to the prodomain of caspase-2 and recruits it to the signalling complex. Cells undergoing apoptosis following triggering of death receptors execute the death programme by activating a hierarchy of caspases, with caspase-8 and possibly caspase-10 being at or near the apex of this apoptotic cascade.

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4,699 citations

"The Involvement of Cysteine Proteas..." refers background in this paper

...Functional analysis of these proteases established the key regulatory role of these proteases in the apoptosis pathway (Cohen, 1997)....
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...Most animal cysteine proteases associated with apoptosis regulation cleave after an aspartic acid (Cohen, 1997); thus, they have been termed caspases....
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Journal Article•DOI•

The oxidative burst in plant disease resistance

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Christopher J. Lamb¹, Richard A. Dixon•Institutions (1)

Salk Institute for Biological Studies¹

01 Jun 1997

TL;DR: Emerging data indicate that the oxidative burst reflects activation of a membrane-bound NADPH oxidase closely resembling that operating in activated neutrophils, which underlies the expression of disease-resistance mechanisms.

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Abstract: Rapid generation of superoxide and accumulation of H2O2 is a characteristic early feature of the hypersensitive response following perception of pathogen avirulence signals. Emerging data indicate that the oxidative burst reflects activation of a membrane-bound NADPH oxidase closely resembling that operating in activated neutrophils. The oxidants are not only direct protective agents, but H2O2 also functions as a substrate for oxidative cross-linking in the cell wall, as a threshold trigger for hypersensitive cell death, and as a diffusible signal for induction of cellular protectant genes in surrounding cells. Activation of the oxidative burst is a central component of a highly amplified and integrated signal system, also involving salicylic acid and perturbations of cytosolic Ca2+, which underlies the expression of disease-resistance mechanisms.

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3,203 citations

"The Involvement of Cysteine Proteas..." refers background in this paper

...In plants, massive oxidative bursts that generate high levels of H2O2 (Legendre et al., 1993) have been observed in response to avirulent pathogens as part of the hypersensitive response (Lamb and Dixon, 1997)....
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..., 1997), in some forms of senescence, and in the hypersensitive response to pathogens and environmental stresses (Greenberg, 1996; Mittler and Lam, 1996; Lamb and Dixon, 1997)....
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...In many systems, sublethal oxidative stress was found to be involved either directly or indirectly in the PCD process (reviewed in Korsmeyer et al., 1995; Payne et al., 1995; Lamb and Dixon, 1997)....
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...In plants, PCD has been implicated in xylogenesis (Fukuda, 1996; Groover et al., 1997), in some forms of senescence, and in the hypersensitive response to pathogens and environmental stresses (Greenberg, 1996; Mittler and Lam, 1996; Lamb and Dixon, 1997)....
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..., 1993) have been observed in response to avirulent pathogens as part of the hypersensitive response (Lamb and Dixon, 1997)....
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Journal Article•DOI•

H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response

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Alex Levine¹, Raimund Tenhaken¹, Richard A. Dixon, Christopher J. Lamb¹•Institutions (1)

Salk Institute for Biological Studies¹

18 Nov 1994-Cell

TL;DR: It is reported here that H2O2 from this oxidative burst not only drives the cross-linking of cell wall structural proteins, but also functions as a local trigger of programmed death in challenged cells and as a diffusible signal for the induction in adjacent cells of genes encoding cellular protectants.

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2,740 citations

"The Involvement of Cysteine Proteas..." refers background or methods in this paper

...In plant systems, it was shown previously that H2O2 treatment induces PCD in soybean and Arabidopsis cell cultures (Levine et al., 1994, 1996; Desican et al., 1998)....
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...Compelling evidence points to the active participation of ROS in plant (Levine et al., 1994; Chamnongpol et al., 1996; Schraudner et al., 1997) and in animal (Korsmeyer et al., 1995) PCD....
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...Cells were grown as described in Levine et al. (1994), except that 6 mL of cells was transferred into 40 mL of fresh medium every 7 days....
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...Suspension-cultured soybean Williams 82 cells were treated with H 2 O 2 at a concentration that was shown to induce PCD (Levine et al., 1994; Desikan et al., 1998), and the cells were harvested at different intervals after the stimulus was applied....
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...Three distinct phases that depend on the concentration of ROS characterize cellular responses to oxidative stress (Dypbukt et al., 1994; Levine et al., 1994)....
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Journal Article•DOI•

The role of active oxygen in the response of plants to water deficit and desiccation.

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Nicholas Smirnoff¹•Institutions (1)

University of Exeter¹

01 Sep 1993-New Phytologist

TL;DR: During normally-encountered degrees of water deficit the capacity of the antioxidant systems and their ability to respond to increased active oxygen generation may be sufficient to prevent overt expression of damage.

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Abstract: Water deficits cause a reduction in the rate of photosynthesis. Exposure to mild water deficits, when relative water content (RWC) remains above 70%, primarily causes limitation to carbon dioxide uptake because of stomatal closure. With greater water deficits, direct inhibition of photosynthesis occurs. In both cases limitation of carbon dioxide fixation results in exposure of chloroplasts to excess excitation energy. Much of this can be dissipated by various photoprotective mechanisms. These include dissipation as heat via carotenoids, photorespiration, CAM idling and, in some species, leaf movements and other morphological features which minimize light absorption. The active oxygen species superoxide and singlet oxygen are produced in chloroplasts by photoreduction of Oxygen and energy transfer from triplet excited chlorophyll to oxygen, respectively. Hydrogen peroxide and hydroxyl radicals can form as a result of the reactions of superoxide. All these species are reactive and potentially damaging, causing lipid peroxidation and inactivation of enzymes. They are normally scavenged by a range of antioxidants and enzymes which are present in the chloroplast and other subcellular compartments. When carbon dioxide fixation is limited by water deficit, the rate of active oxygen formation increases in chloroplasts as excess excitation energy, not dissipated fay the photoprotective mechanisms, is used to form superoxide and singlet oxygen. However, photorespiratory hydrogen peroxide production in peroxisomes decreases. Increased superoxide can be detected by EPR (electron paramagnetic resonance) in chloroplasts from droughted plants. Stiperoxide formation leads to changes suggestive of oxidative damage including lipid peroxidation and a decrease in ascorbate. These changes are not, however, apparent until severe water deficits develop, and they could also be interpreted as secondary effects of water deficit-induced senescence or wounding. Non-lethal water deficits often result in increased activity of superoxide dismutase, glutathione reductase and monodehydroascorbate reductase. Increased capacity of these protective enzymes may be part of a general antioxidative response in plants involving regulation of protein synthesis or gene expression. Since the capacity of these enzymes is also increased by other treatments which cause oxidative damage, and which alter the balance between excitation energy input and carbon dioxide fixation such as low temperature and high irradiance, it is suggested that water deficit has the same effect. Light levels that are not normally excessive do become excessive and photoprotective/antioxidative systems are activated. Some of the photoprotective mechanisms themselves could result in active oxygen formation. Photoinhibitory damage also includes a component of oxidative damage. During normally-encountered degrees of water deficit the capacity of the antioxidant systems and their ability to respond to increased active oxygen generation may be sufficient to prevent overt expression of damage. Desiccation-tolerant tissues such as bryophytes, lichens, spores, seeds, some algae and a few vascular plant leaves can survive desiccation to below 30-40% RWC, A component of desiccation damage in seeds and bacteria is oxygen-dependent. Desiccation causes oxidation of glutathione, a major antioxidant, and appearance of a free radical signal detected by EPR in a number of tissues suggesting that oxidative damage has occurred. In photosynthetic cells damage may arise from photooxidation. Disruption of membrane-bound electron tranport systems in partially hydrated tissue could lead to reduction of oxygen to superoxide. Oxidation of lipids and sulphydryl groups may also occur in dry tissue. Tolerant cells recover upon rehydration and arc able to reduce their glutathione pool. Non-tolerant species go on to show further oxidative damage including lipid peroxidation. It is difficult to attribute this subsequent damage to the cause or effect of death. Embryos in seeds lose desiccation tolerance soon after imbibition. This is associated with membrane damage that has been attributed to superoxide-mediated deesterification of phospholipids and loss of lipophilic antioxidants. These effects are discussed in relation to other mechanisms involved in desiccation tolerance. Contents Summary 27 I. Introduction 28 II. Generation of active oxygen and defence mechanisms in plant cells 29 III. The effect of water deficit on photosynthesis 31 IV. Mechanisms for active oxygen generation during water deficit 36 V. Evidence for oxidative damage during water deficit 39 VI. Desiccation 47 VII. Conclusions 52 Acknowledgements 53 References 53.

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2,008 citations

"The Involvement of Cysteine Proteas..." refers background in this paper

..., 1993), and drought (Smirnoff, 1993) stresses, our results may be important in the future engineering of plant resistance to different environmental stresses by genetically modulating the activity of endogenous protease inhibitor genes....
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...…many of the environmental stresses, such as chilling (Prasad et al., 1994), ozone (Pell et al., 1997), salt (Hernandez et al., 1993), and drought (Smirnoff, 1993) stresses, our results may be important in the future engineering of plant resistance to different environmental stresses by…...
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Journal Article•DOI•

Protease activation during apoptosis: Death by a thousand cuts?

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Seamus J. Martin¹, Douglas R. Green¹•Institutions (1)

La Jolla Institute for Allergy and Immunology¹

11 Aug 1995-Cell

TL;DR: Observations from studies using enucleated cells as well as cell-free systems indicate that the central components of the cell death machinery are most likely localized to the cytosol, and several lines of evidence indicate that proteases, particularly those of the emerging interleukin-lp (IL-lp)converting enzyme (ICE) family, are good candidates for regulators or components (or both) of the executioner.

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1,356 citations

"The Involvement of Cysteine Proteas..." refers background in this paper

...In the animal systems, activation of cysteine proteases has emerged as a key event in the regulation of apoptosis (Martin and Green, 1995)....
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...Activation of cysteine proteases constitutes the critical point in the PCD pathway of animal cells (Earnshaw, 1995; Martin and Green, 1995; Martins et al., 1997)....
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