Chapter 4 - The Botanical Dance of Death: Programmed Cell Death in Plants

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Abstract

Programmed cell death (PCD) describes a small number of processes that result in a highly controlled, and organised, form of cellular destruction, activated in every part of the plant, throughout its entire life cycle. For example, PCD is a critical component of many vegetative and reproductive developmental processes, senescence programmes, pathogen defence mechanisms and stress responses. Cell destruction can manifest as apoptotic-like, necrotic or autophagic cell death, and these processes are likely to overlap extensively, sharing several regulatory mechanisms. Several of the key PCD regulators and signals have now been revealed, for example, many cell organelles, including mitochondria, chloroplasts, Golgi apparatus, endoplasmic reticulum and vacuoles have been shown to have a role in controlling PCD activation. Following activation the actual dismantling of the cell appears to involve cell death proteases including those with caspase-like, or metacaspase, activity. This review will examine the current state of knowledge about the regulation of events during plant PCD. We will describe numerous examples of developmental or environmentally induced deaths and outline their potential as model systems for use in PCD research programmes. Similarly, a range of techniques and in vitro model systems that can be used to identify, and quantify, rates of plant PCD are reviewed. These model systems and techniques can be used to identify the underlying signals and events that drive and regulate PCD and ultimately reveal the steps necessary for the botanical dance of death.

Introduction

Lockshin and Zakeri (2004) defined programmed cell death (PCD) as the sequence of (potentially interruptible) events that lead to the controlled death of the cell. PCD generally describes apoptotic (type I) or autophagic (type II) cell death, in contrast to necrotic (type III) cell death (Bras et al., 2005, Lockshin and Zakeri, 2004). Apoptosis in animal cells is phenotypically characterised by cell shrinkage, nuclear condensation and fragmentation, plasma membrane blebbing and, finally, collapse of the cell into small fragments, apoptotic bodies, which are subsequently removed by phagocytosis (Lennon et al., 1991). Molecular mechanisms of mammalian apoptosis are well understood: cellular dismantling is executed by caspase (Cysteine-dependent ASPartate-directed proteASES) activation (Adrain and Martin, 2001). Caspase activation may be initiated either via an extrinsic pathway which is death receptor mediated, or an intrinsic pathway, which is controlled by the release of pro-apoptotic proteins from mitochondria. In plants, most elements of the PCD machinery remain unknown and, moreover, truly apoptotic morphology (formation of apoptotic bodies) is not universally observed (McCabe et al., 1997a). This is not surprising due to presence of the plant's cell wall, preventing final clearance by phagocytosis by adjacent cells. Consequently, in order to acknowledge similarities between plant PCD and apoptosis while recognising differences between them, the term ‘apoptotic-like PCD’ (AL-PCD) was introduced (Danon et al., 2000). AL-PCD describes a type of plant cell death pathway which is characterised by DNA degradation and condensation of the protoplast away from the cell wall (Fig. 1), similar to the apoptotic morphology seen in animal cells (McCabe and Leaver, 2000, McCabe et al., 1997a, Reape and McCabe, 2008, Reape and McCabe, 2010). Autophagic cell death, on the other hand, occurs without chromatin condensation and is accompanied by massive autophagic vacuolisation of the cytoplasm (Kroemer et al., 2008), while necrosis is often described as unorganised cell destruction process which occurs following overwhelming stress. During necrosis, the cell loses its ability to osmoregulate which results in water and ion influx and swelling of the cell membrane and organelles (Lennon et al., 1991, Lockshin and Zakeri, 2004). Until recently, necrosis has been considered a passive and accidental cellular event, but recent data suggest that in certain cases this process can be programmed and controlled to a certain extent (Festjens et al., 2006, Golstein and Kroemer, 2007). Similarities between the cell death programmes seen in animal and plant cells such as conservation of autophagic genes or apoptotic cell shrinkage, chromatin condensation, DNA fragmentation and mitochondrial release of cytochrome c (cyt c) suggest that at least some death mechanisms are conserved throughout the plant and animal kingdoms, having been derived from ancestral unicellular death programmes.

PCD is a broad term describing multiple, possibly overlapping death pathways operating in eukaryotic cells. New types of organised cell death are being described and the terminology referring to PCD is constantly expanding (Kroemer et al., 2008). It seems unlikely that a definite and unconditional distinction between different forms of cell death, based only on morphological criteria, can be established, as dying cells often display mixed cell death morphologies (Martin and Baehrecke, 2004, Nicotera and Melino, 2004). The contribution to a particular cell death pathway by specific cellular death machinery is still being defined. It is therefore important to introduce a non-rigid, but uniform, nomenclature and if possible give details (e.g. in terms of time, morphology, and presence of different markers) defining the specific type of cell death under investigation, rather than simply referring to the process as PCD (Reape and McCabe, 2008). In the case of plant cells, clear descriptions of the processes examined are particularly important, especially as the mechanisms of plant PCD are far less understood compared to the animal kingdom. Nomenclature and definitions created and used traditionally for description of cell death in animal cells may not always be adequate for plant-focused research and their misuse may result in confusion and incorrect interpretation of data. Therefore it is advisable that experimental data are carefully analysed with special focus put on the methodology and experimental design used by the researchers. For example, the presence of hallmark features of AL-PCD, such as cyt c release or DNA laddering, should be monitored throughout the course of the cell death process rather than at one particular time point. Further, if cell death is induced by application of external stimuli, the magnitude of the stress applied has to be carefully selected to ensure that it is sufficient to induce PCD, but not so high that it is overwhelming and results in necrosis (McCabe et al. 1997a). One should also critically consider the assays used to investigate different instances of PCD and be aware of both the advantages and drawbacks of each particular assay. For example, monodansylcadaverine (MDC) has been considered an autophagy-specific marker but its specificity is now being questioned (see Section IV) and sample preparation procedures have occasionally been shown to affect the outcome of a PCD biochemical assay, such as terminal deoxynucleotidyl transferase dUTP nick end labelling (TUNEL; Wang et al., 1996).

The optimal means of communicating results concerning cell death events in plants is to provide the scientific audience with comprehensive descriptions of morphology, biochemistry and timing-related data, rather than using PCD as the general term describing the whole death process. In this review, while examining diverse examples of plant PCD, we have endeavoured to describe the characteristic features and events accompanying the type of cell death under consideration.

Section snippets

Mitochondria and Chloroplasts

Although the regulation of plant PCD has been a subject of intensive research, the sequence of events leading to organised cell death has only begun to emerge. Due to the assumed evolutionary conservation of at least some elements of the PCD machinery, significant research efforts have focused on examining the similarities between PCD programmes in animal and plant cells. In animal cells, apoptosis can be activated either through the intrinsic or extrinsic pathway. The intrinsic pathway is

Role of PCD in Developmental, Defence and Stress Responses

PCD is an essential component of complex multicellular body plan formation. The following sections serve to illustrate how developmentally regulated, and environmentally induced, changes in plant structure cannot be accomplished without PCD mediating the remodelling of cells and tissues.

Autophagy

Autophagy is an evolutionary conserved catabolic pathway in eukaryotes in which cytoplasm, including long-lived proteins and obsolete organelles, are sequestered into double-membrane vesicles (autophagosome) and delivered to the degradative organelle (in plants, the vacuole) for breakdown and final recycling of the resulting macromolecules (Yorimitsu and Klionsky, 2005). This sequestration process can occur either away from the vacuole (in which case it is termed macroautophagy) or at the

Methods

PCD in plants can be measured by microscopic and biochemical assays. Microscopic examination of PCD includes application of viability stains such as fluorescein diacetate, Evans blue or tryptan blue and use of in situ markers of DNA degradation such as the TUNEL, which provides a measure of 3′-OH group accumulation (Gavrieli et al., 1992) and the 4′,6-diamidino-2-phenylindole (DAPI) staining, which specifically targets DNA located in the nuclei. It is often useful to use more than one PCD

Conclusions

The decision of a cell to undergo PCD is the outcome of a complex signalling process. Although pathways governing this decision are less clear for plant than for animal cells, the sequence of events leading to plant PCD is starting to emerge. Through the study of PCD occurrences throughout the plant life cycle, a diverse set of characteristics that specifically define plant PCD have been identified. However, several but not all of these features are shared with animal apoptosis. Unique

Acknowledgements

We wish to thank Dr. Theresa J. Reape for critical reading. JK and CTD are funded by The Embark Initiative, a Government of Ireland scholarship operated by The Irish Research Council for Science, Engineering and Technology.

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