Programmed cell death in plants

The modern concepts of programmed cell death (PCD) in plants are reviewed as compared to PCD (apoptosis) in animals. Special attention is focused on considering the potential mechanisms of implementation of this fundamental biological process and its participants. In particular, the proteolytic enzymes involved in PCD in animals (caspases) and plants (phytaspases) are compared. Emphasis is put on elucidation of both common features and substantial differences of PCD implementation in plants and animals.     

Programmed cell death in plants: Protective effect of tetraphenylphosphonium and tetramethylrhodamine cations used as transmembrane quinone carriers

Tetraphenylphosphonium (TPP⁺) and tetramethylrhodamine ethyl ester (TMRE⁺) cations used as transmembrane carriers of ubiquinone (MitoQ) and plastoquinone (SkQ, SkQR) in mitochondria prevented at nanomolar concentrations the chitosanor H₂O₂-induced destruction of the nucleus in epidermal cells of epidermis isolated from pea leaves. The protective effect of the cations was potentiated by palmitate. Penetrating anions of tetraphenylboron (TB⁻) and phenyl dicarbaundecaborane also displayed protective effects at micromolar concentrations; the effect of TB⁻ was potentiated by NH₄Cl. It is proposed that the protective effect of the penetrating cations and anions against chitosan is due to suppression of the generation of reactive oxygen species in mitochondria as a result of the protonophoric effect of the cations plus fatty acids and the anions plus NH₄⁺. Phenol was suitable as the electron donor for H₂O₂ reduction catalyzed by horseradish peroxidase, preventing the destruction of cell nuclei. The penetrating cations and anions, SkQ1, and SkQR1 did not maintain the peroxidase or peroxidase/oxidase reactions measured by their suitability as electron donors for H₂O₂ reduction or by the oxidation of exogenous NADH.     

Programmed cell death and tissue remodelling in plants

The use of programmed cell death (PCD) to remodel plants at the cellular, tissue, and organ levels is particularly fascinating and occurs in such processes as tracheary element differentiation, lysigenous aerenchyma formation, development of functionally unisexual flowers from bisexual floral primordia, and leaf morphogenesis. The formation of complex leaf shape through the use of PCD is a rare event across vascular plants and occurs only in a few species of Monstera and related genera, and in the lace plant (Aponogeton madagascariensis). During early development, the lace plant leaf forms a pattern of equidistantly positioned perforations across the surface of the leaf, giving it a lattice-like appearance. Due to the accessibility and predictability of this process, the lace plant provides highly suitable material for the study of developmentally regulated PCD in plants. A sterile lace plant culture system has been successfully established, providing material free of micro-organisms for experimental study. The potential role of ethylene and caspase-like activity in developmentally regulated PCD in the lace plant is currently under investigation, with preliminary results indicating that both may play a role in the cell death pathway.     

Programmed cell death in plants: distinguishing between different modes

Programmed cell death (PCD) in plants is a crucial componentof development and defence mechanisms. In animals, differenttypes of cell death (apoptosis, autophagy, and necrosis) havebeen distinguished morphologically and discussed in these morphologicalterms. PCD is largely used to describe the processes of apoptosisand autophagy (although some use PCD and apoptosis interchangeably)while necrosis is generally described as a chaotic and uncontrolledmode of death. In plants, the term PCD is widely used to describemost instances of death observed. At present, there is a vastarray of plant cell culture models and developmental systemsbeing studied by different research groups and it is clear fromwhat is described in this mass of literature that, as with animals,there does not appear to be just one type of PCD in plants.It is fundamentally important to be able to distinguish betweendifferent types of cell death for several reasons. For example,it is clear that, in cell culture systems, the window of timein which ‘PCD’ is studied by different groups varieshugely and this can have profound effects on the interpretationof data and complicates attempts to compare different researcher'sdata. In addition, different types of PCD will probably havedifferent regulators and modes of death. For this reason, inplant cell cultures an apoptotic-like PCD (AL-PCD) has beenidentified that is fairly rapid and results in a distinct corpsemorphology which is visible 4–6 h after release of cytochromec and other apoptogenic proteins. This type of morphology, distinctfrom autophagy and from necrosis, has also been observed inexamples of plant development. In this review, our model systemand how it is used to distinguish specifically between AL-PCDand necrosis will be discussed. The different types of PCD observedin plants will also be discussed and the importance of distinguishingbetween different forms of cell death will be highlighted. Key words: Apoptosis, apoptosis-like programmed cell death (AL-PCD), Arabidopsis, autophagy, mitochondria, necrosis, programmed cell death (PCD) Received 5 June 2007; Revised 13 September 2007 Accepted 20 September 2007     

Programmed cell death in plants under anaerobic conditions: Effect of Ag+

We investigated epidermal peels from the leaves of pea (Pisum sativum L.) consisting of a monolayer of the cells of two types: stomatal guard cells (GC) with chloroplasts and mitochondria and basic epidermal cells (EC) containing only mitochondria. As inducers of programmed cell death, we used KCN destroying the nuclei in GC and EC and chitosan that destroys nuclei only in EC. AgNO₃ (10 μM) stimulated the destruction of nuclei in GC and EC induced by CN^? and suppressed chitosan-induced destruction of nuclei in EC. The destruction of nuclei in GC induced by CN^? occurred under aerobic conditions and was prevented under anaerobiosis. The destruction of nuclei in GC induced by (CN^? + Ag⁺) occurred both under aerobic and anaerobic conditions and was not suppressed by antioxidants. Among the tested cations of metals (Ag+, Hg²⁺, Fe²⁺, Fe³⁺, Cu²⁺, and Mn²⁺), Ag⁺ turned out to be the most efficient in respect to the stimulation of cyanide-induced destruction of nuclei in GC. Half-maximum concentrations of Ag⁺ and Hg²⁺ were equal to 4–5 μM. In epidermal peels treated with chitosan, GC were permeable to propidium iodide; however, the nuclei in GC (in contrast to EC) were not destructed in the presence of chitosan. It was concluded that Ag⁺, acting as an electron acceptor during photosynthetic electron transfer in the chloroplasts from pea leaves, impeded the O₂ evolution by the chloroplasts treated with ferricyanide or silicomolybdate as electron acceptors, impeded the consumption of O₂ in the course of electron transfer from the (ascorbate + N,N,N′,N′-tetramethyl-p-phenylenediamine) to methylviologen and suppressed the production of reactive oxygen species (ROS) in GC and EC.     

Programmed cell death of tracheary elements as a paradigm in plants

Plant development involves various programmed cell death (PCD) processes. Among them, cell death occurring during differentiation of procambium into tracheary elements (TEs), which are a major component of vessels or tracheids, has been studied extensively. Recent studies of PCD during TE differentiation mainly using an in vitro differentiation system of Zinnia have revealed that PCD of TEs is a plant-specific one in which the vacuole plays a central role. Furthermore, there are recent findings of several factors that may initiate PCD of TEs and that act at autonomous degradation of cell contents. Herein I summarize the present knowledge about cell death program during TE differentiation as an excellent example of PCD in plants.     

Programmed cell death

This paper reviews data on programmed cell death (apoptosis) in animals and plants. Necrosis is a pathological scenario of cell death, which entails an inflammatory response in animal tissues. Apoptosis results in the disintegration of animal/plant cells into membrane vesicles enclosing the intracellular content, which are thereupon engulfed by adjacent or specialized cells (phagocytes) in animals. Plants lack such specialized cells, and plant cell walls prevent phagocytosis. The paper considers the main molecular mechanisms of apoptosis in animals and the pathways of activation of caspases, evolutionarily conserved cysteine proteases. A self-contained section concerns itself with the process of programmed cell death (PCD) in microorganisms including: 1) cell death in the myxomycete Dictyostelium discoideum and the parasitic flagellate Trypanosoma cruzi; 2) PCD in genetically manipulated yeast expressing the proapoptotic Bax and Bak proteins; 3) the death of a part of a prokaryotic cell population upon the depletion of nutrient resources or under stress; 4) the elimination of cells after a loss of a plasmid encoding a stable cytotoxic agent in combination with an unstable antidote; and 5) PCD in phage-infected bacterial cells.     

Programmed cell death in cell cultures

In plants most instances of programmed cell death (PCD) occur in a number of related, or neighbouring, cells in specific tissues. However, recent research with plant cell cultures has demonstrated that PCD can be induced in single cells. The uniformity, accessibility and reduced complexity of cell cultures make them ideal research tools to investigate the regulation of PCD in plants. PCD has now been induced in cell cultures from a wide range of species including many of the so-called model species. We will discuss the establishment of cell cultures, the fractionation of single cells and isolation of protoplasts, and consider the characteristic features of PCD in cultured cells. We will review the wide range of methods to induce cell death in cell cultures ranging from abiotic stress, absence of survival signals, manipulation of signal pathway intermediates, through the induction of defence-related PCD and developmentally induced cell death.     

Programmed cell death in bacteria

Programmed death (PDC) of individual cells is a genetically controlled biological process related to the development of multicellular organisms. It proceeds in most cases as apoptosis characterized by DNA degradation and breakdown of dying cells to apoptotic bodies, and ending by their phagocytosis by macrophages or by the surrounding tissue. Unlike apoptosis, necrosis is a genetically unregulated sudden death of a group of cells caused by a severe damage of membranes and other cell components. In bacteria, programmed cell death is mostly related to population development. This holds mainly for sporulation of bacilli where the process is best understood at the morphological, physiological and genetic level. Sporulation of bacilli begins by an asymmetric division of the nongrowing cell into two parts—the mother and the forespore compartment, whose fate is different. Whereas the smaller compartment develops into the spore, the function of the larger is twofold. It participates in the spore development mainly by forming spore coast but it also synthesizes or activates the autolytic apparatus which lyzes the sporangium cell wall at the end of the process. Some phases of the development of myxobacteria and streptomycetes also have characteristic features of programmed death. Unlike sporulation of bacilli, the autolysis of a portion of population of myxobacteria or hyphae of streptomycetes proceeds in the middle of their developmental cycle. Extensive turnover of cell membranes in growing myxobacteria results in the formation of a fatty acid mixture—theautocide—which kills a smaller or greater portion of the myxobacterial population. The dead cells are digested by extracellular enzymes released by myxobacteria and the digest is used as nutrient for completion of the developmental cycle of the remaining living population. Similar events take place also during the formation of aerial mycelium in streptomycetes. Here the autolysis of a portion of vegetative (substrate) mycelium supplies amino acids for the formation of aerial mycelium. The recently discovered programmed death of plasmid-free descendants of a plasmid-bearing population of different bacteria is based on the loss of control of toxin activity by its antidote. Both substances are encoded by plasmid DNA and the loss of the plasmid results in an “enforced suicide” of the host cell because the effective concentration of the antidote decreases more rapidly than that of the toxin. The mechanisms of this suicide can vary. In addition to the above mentioned kinds of programmed death, other events of developmentally regulated death of prokaryotes probably exist. Some bacteria contain “death genes” in their chromosome which trigger cell death at the onset of the stationary phase. The physiological function of this kind of suicide is not known. However, most nonsporulating bacteria developed a strategy of surviving at the nongrowing stage by transforming the growing cell to a more resistant dormant (cryptobiological) form.     

Programmed cell death in protists

Programmed cell death in protists does not seem to make sense at first sight. However, apoptotic markers in unicellular organisms have been observed in all but one of the six/eight major groups of eukaryotes suggesting an ancient evolutionary origin of this regulated process. This review summarizes the available data on apoptotic markers in non-opisthokonts and elucidates potential functions and evolution of programmed cell death. A newly discovered family of caspase-like proteases, the metacaspases, is considered to exert the function of caspases in unicellular organisms. Important results on metacaspases, however, showed that they cannot be always correlated to the measured proteolytic activity during protist cell death. Thus, a major challenge for apoptosis research in a variety of protists remains the identification of the molecular cell death machinery.     

Programmed cell death lives

Research on cell death mechanisms gets a lot of attention. This is understandable as it underlies biology in general, as well as the insight in pathological conditions and the development of opportunities for therapeutic intervention. Over the last years a steady rise in the number of scientific reports and in the impact of this literature on the different mechanisms of programmed cell death can be observed. A number of new concepts are highlighted.

     

Programmed cell death in trypanosomatids

It has generally been assumed that apoptosis and other forms of programmed cell death evolved to regulate growth and development in multicellular organisms. However, recent work has shown that some parasitic protozoa have evolved a cell suicide pathway analogous to the process described as apoptosis in metazoa. In this review, Susan Welburn, Marcello Barcinski and Gwyn Williams discuss the possible implications of a cell suicide pathway in the vector-borne Trypanosomatids.     

Programmed cell death in Giardia

Programmed cell death (PCD) has been observed in many unicellular eukaryotes; however, in very few cases have the pathways been described. Recently the early divergent amitochondrial eukaryote Giardia has been included in this group. In this paper we investigate the processes of PCD in Giardia. We performed a bioinformatics survey of Giardia genomes to identify genes associated with PCD alongside traditional methods for studying apoptosis and autophagy. Analysis of Giardia genomes failed to highlight any genes involved in apoptotic-like PCD; however, we were able to induce apoptotic-like morphological changes in response to oxidative stress (H2O2) and drugs (metronidazole). In addition we did not detect caspase activity in induced cells. Interestingly, we did observe changes resembling autophagy when cells were starved (staining with MDC) and genome analysis revealed some key genes associated with autophagy such as TOR, ATG1 and ATG 16. In organisms such as Trichomonas vaginalis, Entamoeba histolytica and Blastocystis similar observations have been made but no genes have been identified. We propose that Giardia possess a pathway of autophagy and a form of apoptosis very different from the classical known mechanism; this may represent an early form of programmed cell death.     

Programmed cell death: similarities and differences in animals and plants. A flower paradigm

Summary. After an overview of the criteria for the definition of cell death in the animal cell and of its different types of death, a comparative analysis of PCD in the plant cell is reported. The cytological characteristics of the plant cell undergoing PCD are described. The role of plant hormones and growth factors in the regulation of this event is discussed with particular emphasis on PCD activation or prevention by polyamine treatment (doses, timing and developmental stage of the organism) in a Developmental cell death plant model: the Nicotiana tabacum (tobacco) flower corolla. Some of the effects of polyamines might be mediated by transglutaminase catalysis. The activity of this enzyme was examined in different parts of the corolla during its life span showing an acropetal trend parallel to the cell death wave. The location of transglutaminase in some sub-cellular compartments suggests that it exerts different functions in the corolla DCD.     

Programmed cell death in fission yeast

Recently a metacaspase, encoded by YCA1, has been implicated in a primitive form of apoptosis or programmed cell death in yeast. Previously it had been shown that over-expression of mammalian pro-apoptotic proteins can induce cell death in yeast, but the mechanism of how cell death occurred was not clearly established. More recently, it has been shown that DNA or oxidative damage, or other cell cycle blocks, can result in cell death that mimics apoptosis in higher cells. Also, in fission yeast deletion of genes required for triacylglycerol synthesis leads to cell death and expression of apoptotic markers. A metacaspase sharing greater than 40% identity to budding yeast Yca1 has been identified in fission yeast, however, its role in programmed cell death is not yet known. Analysis of the genetic pathways that influence cell death in yeast may provide insights into the mechanisms of apoptosis in all eukaryotic organisms.     

Programmed cell death in cereal aleurone

Progress in understanding programmed cell death (PCD) in the cereal aleurone is described. Cereal aleurone cells are specialized endosperm cells that function to synthesize and secrete hydrolytic enzymes that break down reserves in the starchy endosperm. Unlike the cells of the starchy endosperm, aleurone cells are viable in mature grain but undergo PCD when germination is triggered or when isolated aleurone layers or protoplasts are incubated in gibberellic acid (GA). Abscisic acid (ABA) slows down the process of aleurone cell death and isolated aleurone protoplasts can be kept alive in media containing ABA for up to 6 months. Cell death in barley aleurone occurs only after cells become highly vacuolated and is manifested in an abrupt loss of plasma membrane integrity. Aleurone cell death does not follow the apoptotic pathway found in many animal cells. The hallmarks of apoptosis, including internucleosomal DNA cleavage, plasma membrane and nuclear blebbing and formation of apoptotic bodies, are not observed in dying aleurone cells. PCD in barley aleurone cells is accompanied by the accumulation of a spectrum of nuclease and protease activities and the loss of organelles as a result of cellular autolysis.     

Programmed cell death in pathogenic fungi

Greater understanding of programmed cell death (PCD) responses in pathogenic fungi may offer a chance of exploiting the fungal molecular death machinery to control fungal infections. Clearly identifiable differences between the death machineries of pathogens and their hosts, make this a feasible target. Evidence for PCD in a range of pathogenic fungi is discussed alongside an evaluation of the capacity of existing antifungal agents to promote apoptosis and other forms of cell death. Information about death related signalling pathways that have been examined in pathogens as diverse as Candida albicans, Aspergillus fumigatus, Magnaporthe grisea and Colletotrichum trifolii are discussed.