Regulation and execution of programmed cell death in response to pathogens, stress and developmental cues

Beers, Eric P.; McDowell, John M.

doi:10.1016/s1369-5266(00)00216-8

Cited by 171 publications

(138 citation statements)

References 62 publications

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“…43,44 Although autolytic components appear to be important for the HR cell death in some cases that have been studied, collapse of lytic vacuoles during the HR does not lead to complete clearance of the protoplast, as it does in vacuolar PCD. 39,45 When discussing the relationship of the HR cell death to its correlated cytological features, and ultimately to the restriction of pathogen success, it is important to consider where the pathogens proliferate: for example, bacterial pathogens proliferate in the apoplast, outside the cell, while viruses proliferate within cells. Thus, vacuolar collapse can be effective to restrict viral pathogens, 10 while discharge of defense proteins into the apoplast, accompanied by fusion of the tonoplast and plasma membrane, slows bacterial pathogens outside the cells.…”

Section: Mixed and Atypical Modalities Of Plant Cell Deathmentioning

confidence: 99%

Morphological classification of plant cell deaths

et al. 2011

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Programmed cell death (PCD) is an integral part of plant development and of responses to abiotic stress or pathogens. Although the morphology of plant PCD is, in some cases, well characterised and molecular mechanisms controlling plant PCD are beginning to emerge, there is still confusion about the classification of PCD in plants. Here we suggest a classification based on morphological criteria. According to this classification, the use of the term 'apoptosis' is not justified in plants, but at least two classes of PCD can be distinguished: vacuolar cell death and necrosis. During vacuolar cell death, the cell contents are removed by a combination of autophagy-like process and release of hydrolases from collapsed lytic vacuoles. Necrosis is characterised by early rupture of the plasma membrane, shrinkage of the protoplast and absence of vacuolar cell death features. Vacuolar cell death is common during tissue and organ formation and elimination, whereas necrosis is typically found under abiotic stress. Some examples of plant PCD cannot be ascribed to either major class and are therefore classified as separate modalities. These are PCD associated with the hypersensitive response to biotrophic pathogens, which can express features of both necrosis and vacuolar cell death, PCD in starchy cereal endosperm and during self-incompatibility. The present classification is not static, but will be subject to further revision, especially when specific biochemical pathways are better defined. Research on plant cell death has grown considerably in the past few years, owing to the importance of cell death for plant development and defense. Just as animal cells engage several mechanisms leading to death, the road to cell demise in plants can also vary. The long evolutionary distance and distinct cellular architecture between the two kingdoms may account for the differences between the mechanisms of plant and animal cell death. It is therefore appropriate to assess the relevance of animal cell death nomenclature 1 to plants. At present, there is confusion in cell death terminology in plant biology, which drives our attempt to formulate a more logical classification. Although our molecular understanding of plant cell death regulation and execution is insufficient to create definitive classifications based on precise biochemical pathways, it is possible to begin classifying plant cell death scenarios based on morphological criteria, as was initially the case in animal cell death research 2,3 and is still used for the classification of cell death in animal science. 1 This document attempts to provide a classification of plant cell death. We urge authors, reviewers and editors to follow this classification to facilitate communication between scientists and accelerate research in this field.

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Section: Mixed and Atypical Modalities Of Plant Cell Deathmentioning

confidence: 99%

Morphological classification of plant cell deaths

et al. 2011

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“…While research of mitochondrial bioenergetics and biogenesis continues unabated, a new area of investigation has developed in recent years that centres on the role of this ubiquitous eukaryotic organelle in intracellular stress sensing and programmed cell death (see Beers and McDowell 2001, Desagher and Martinou 2000, Jabs 1999, Jones 2000, Kamata and Hirata 1999. As a central site of metabolism, the mitochondrion is able to integrate many aspects of cell function, and thus, the functional state of this organelle may represent a vital mechanism the cell uses to maintain homeostasis, and as a consequence, a key site where various stresses may become integrated and appropriate acclimatory response co-ordinated.…”

Section: Introductionmentioning

confidence: 99%

Characterization of the alternative oxidase of Chlamydomonas reinhardtii in response to oxidative stress and a shift in nitrogen source

Molen

Rosso

Piercy

et al. 2006

Physiologia Plantarum

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To study the transcriptional regulation of Aox1, the major alternative oxidase (AOX) gene, we fused 1072 bp of its promoter to the promoterless arylsulfatase reporter gene. We find that the reporter is strongly activated when cells are shifted from a medium containing ammonium to one containing nitrate but is unresponsive to treatments known to induce Aox1 in higher plants -H 2 O 2 , antimycin A and cold stress. However, induction of Aox1 by all these factors was found when changes in gene expression were monitored using RNA blot analysis. Our data suggest that transcriptional upregulation of Aox1 by H 2 O 2 , antimycin A and cold-stress requires one or more enhancers which are not found in the proximal promoter region of the gene. Interestingly, while nitrate, H 2 O 2 and cold stress result in increased AOX abundance and increased alternative pathway respiration, these changes are not seen when cells are treated with antimycin A. We find that H 2 O 2 , antimycin A and cold-stress result in an increase in intracellular reactive oxygen species (ROS) but that a significant change in ROS does not occur when cells are shifted into a medium-containing nitrate. Overall, our data are consistent with there being two distinct pathways regulating Aox1 transcription and AOX abundance in Chlamydomonas reinhardtii: one in response to oxidative stress and a second due to metabolic changes brought about by a shift in nitrogen source from ammonium to nitrate.

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“…In spite of the growing list of examples of developmental cell death in plants (reviewed in ref. 1 ), very little is known about its mechanisms. Direct search for the plant orthologs of the core apoptotic cell-death proteins has shown that neither Bcl-2 family members, nor Apaf-1-related proteins or canonical caspases are present in plants.…”

Section: Introductionmentioning

confidence: 99%

“…2,3 Furthermore, numerous cytological observations suggest that plants employ a nonapoptotic pathway of cell dismantling defined as autophagic cell death. 1,4 The hallmark feature distinguishing this type of cell death from apoptosis is that complete cellular degradation takes place inside the dying cell itself without active participation of phagocytes. 5 Notwithstanding a lack of direct plant homologs of mammalian caspases, the possibility that plants may possess enzymes with caspase-like function during programmed cell death has recently commanded the attention of cell death researchers.…”

Section: Introductionmentioning

confidence: 99%

VEIDase is a principal caspase-like activity involved in plant programmed cell death and essential for embryonic pattern formation

et al. 2003

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Plant embryogenesis is intimately associated with programmed cell death. The mechanisms of initiation and control of programmed cell death during plant embryo development are not known. Proteolytic activity associated with caspase-like proteins is paramount for control of programmed cell death in animals and yeasts. Caspase family of proteases has unique strong preference for cleavage of the target proteins next to asparagine residue. In this work, we have used synthetic peptide substrates containing caspase recognition sites and corresponding specific inhibitors to analyse the role of caspase-like activity in the regulation of programmed cell death during plant embryogenesis. We demonstrate that VEIDase is a principal caspase-like activity implicated in plant embryogenesis. This activity increases at the early stages of embryo development that coincide with massive cell death during shape remodeling. The VEIDase activity exhibits high sensitivity to pH, ionic strength and Zn 2 þ concentration. Altogether, biochemical assays show that VEIDase plant caspase-like activity resembles that of both mammalian caspase-6 and yeast metacaspase, YCA1. In vivo, VEIDase activity is localised specifically in the embryonic cells during both the commitment and in the beginning of the execution phase of programmed cell death. Inhibition of VEIDase prevents normal embryo development via blocking the embryo-suspensor differentiation. Our data indicate that the VEIDase activity is an integral part in the control of plant developmental cell death programme, and that this activity is essential for the embryo pattern formation.

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Regulation and execution of programmed cell death in response to pathogens, stress and developmental cues

Cited by 171 publications

References 62 publications

Morphological classification of plant cell deaths

Morphological classification of plant cell deaths

Characterization of the alternative oxidase of Chlamydomonas reinhardtii in response to oxidative stress and a shift in nitrogen source

VEIDase is a principal caspase-like activity involved in plant programmed cell death and essential for embryonic pattern formation

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