ABSTRACT 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.

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. SIMILAR CONTENT BEING VIEWED BY OTHERS DYING IN SELF-DEFENCE: A COMPARATIVE OVERVIEW OF IMMUNOGENIC CELL DEATH SIGNALLING IN ANIMALS AND PLANTS Article Open access 04 October 2022

AC-DEVD-CHO (CASPASE-3/DEVDASE INHIBITOR) SUPPRESSES SELF-INCOMPATIBILITY–INDUCED PROGRAMMED CELL DEATH IN THE POLLEN TUBES OF PETUNIA (_PETUNIA HYBRIDA_ E. VILM.) Article Open access 30

January 2024 ORGANIZED DISASSEMBLY OF PHOTOSYNTHESIS DURING PROGRAMMED CELL DEATH MEDIATED BY LONG CHAIN BASES Article Open access 25 June 2020 MAIN 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 nomenclature1 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 research2, 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. ABSENCE OF APOPTOSIS IN PLANTS Apoptosis is

one of the three major types of cell death found in animals. Compared with the other two – autophagic cell death and necrosis – apoptosis is much better understood, both cytologically and

biochemically.1, 4 Apoptosis is accompanied by rounding up of the cell, reduction of cellular volume, chromatin condensation, nuclear segmentation and very little ultrastructural

modification of cytoplasmic organelles. Its hallmark is blebbing of the plasma membrane (which maintains its integrity until the final stages of apoptosis), followed by fragmentation of the

cell into smaller parcels called apoptotic bodies. Finally, the apoptotic bodies are engulfed by phagocytes and degraded by lysosomal enzymes. This is critical to prevent subsequent

induction of inflammation due to leakage of dead cell contents. The term ‘apoptosis’ should be applied exclusively to cell death that manifests these morphological features. Although

apoptosis is often associated with activation of caspases and oligonucleosomal fragmentation of DNA, these processes can also take place during non-apoptotic cell death, and are thus

insufficient criteria for assignment.1 Plant cells do not exhibit ‘classic’ apoptosis for the following reasons. First, rigid cell walls preclude the necessity for breakdown of the plant

cells into apoptotic bodies. Second, there are no phagocytic cells. A considerable number of articles describing ‘plant apoptosis’ or ‘apoptotic-like programmed cell death (PCD)’ have

nevertheless been published. Critical analysis of this literature reveals three major points that indicate misuse of the term ‘apoptosis’. First, chromatin condensation and DNA fragmentation

are often quoted as apoptotic features. However, neither is specific to apoptosis, because they can also be observed during necrosis and autophagic death.5, 6, 7 Second, stress treatments

often induce shrinkage of the plant protoplast, but not of the cell itself, which can be morphologically reminiscent of apoptotic cell shrinkage. However, animal cells that shrink during

apoptosis maintain their plasma membrane integrity to form apoptotic bodies,8 whereas plant protoplasts that shrink in response to stress usually have damaged plasma membranes and do not

fragment further into discrete bodies.9 Third, increased caspase-like proteolytic activities (in most cases unlinked to specific proteases) in dying plant cells have been used as an argument

for the existence of plant apoptosis. This is an insufficient criterion because activation of caspases _per se_ does not always lead to apoptosis in animal cells.7 Furthermore, the

activation of plant proteases that possess caspase-like activity has not been shown to lead to apoptotic morphology.10, 11, 12 DEFINITION OF ‘VACUOLAR’ PLANT CELL DEATH Plants have elaborate

vacuolar systems that, in contrast to animal lysosomes, can occupy most of the plant cell volume.13 Similar to the roles of lysosomes in animals, plants also use lytic vacuoles to recycle

parts of their cells during normal development and during nutritional stress.14 These lytic vacuoles acquire an important function in one major class of plant cell death, which we recommend

be termed ‘vacuolar cell death’.15 Vacuolar cell death is often manifested by a gradual decrease in the volume of the cytoplasm and a concomitant increase in the volume occupied by lytic

vacuoles (Figure 1). Engulfment of the cytoplasm by lytic vacuoles with subsequent cargo degradation is a major mechanism of cell dismantling during vacuolar cell death. Electron micrographs

often show invaginations in the vacuolar membrane (tonoplast) and fusion of vesicles with the vacuole, followed by uptake and degradation of portions of the cytoplasm in the vacuolar lumen.

This process resembles micro- or macro-autophagy.16, 17, 18, 19, 20 The final step in the execution of vacuolar cell death is rupture of the tonoplast, and a massive release of vacuolar

hydrolases. These rapidly destroy the entire protoplast or in some cases even the entire cell including the cell wall. Other morphological events during vacuolar cell death include formation

of actin cables, nuclear envelope disassembly and, in some examples, nuclear segmentation. The remaining mitochondria and other organelles, as well as the plasma membrane, remain

morphologically intact until rupture of the tonoplast (Table 1; Figure 1). A robust approach to diagnose vacuolar cell death would combine electron microscopy (EM) with the analysis of

autophagic activity, requirement for vacuolar processing enzymes (VPE) and cytoskeletal changes (Table 2). Execution of vacuolar cell death may be a slow process that can take several days

until the rupture of the tonoplast that accomplishes protoplast clearance.18, 19, 20, 21 Depending on the system, the cell wall can be largely degraded, as for example during aerenchyma

formation, leaf perforations in the lace plant and petal senescence22, 23, 24 or can remain intact, for example, during xylem differentiation in vascular plants or leaf remodelling in

_Monstera_ (Figure 1).24, 25, 26 Examples of vacuolar cell death are found during embryo, organ and tissue morphogenesis and senescence, and include, in addition to those mentioned above,

the formation of embryo-suspensor, pollen, ovary, ducts and laticifers.19 Knockout of _ATG_ genes was shown to accelerate _Arabidopsis_ leaf senescence,27, 28 and _ATG5_ has recently been

found to be required for vacuolar cell death of _Arabidopsis_ tracheary elements.29 More extensive work is still needed to determine whether or not _ATG_-dependent autophagic pathways are

required for the execution of vacuolar cell death. DEFINITION OF ‘NECROTIC’ PLANT CELL DEATH Necrosis of animal cells is defined morphologically by the lack of apoptotic or autophagic

features, and positively by the frequent occurrence of an initial gain in cell volume, swelling of various organelles, early rupture of the plasma membrane and loss of intracellular

content.1, 30 Although it is no longer considered to be an unprogrammed process, necrosis remains poorly characterised at the biochemical and genetic levels, so there are as yet no molecular

markers for it. In animal systems, necrosis is often preceded by an increase in cytosolic calcium ion concentration ([Ca2+]cyt), lipid degradation and activation of calpain family

proteases. Mitochondria and lysosomes have been implicated in the downstream events. Mitochondrial changes include uncoupling of respiration, the production of reactive oxygen species (ROS)

and nitrogen species (RNS), a drop in ATP level and mitochondrial membrane permeabilisation (MMP). Lysosomal events include ROS production and permeabilisation of the lysosomal membrane

causing release of active cathepsin proteases to the cytosol.1, 31 Cell death with many of the above characteristics occurs widely in plants. It is induced by a range of abiotic stresses and

by successful recognition of a pathogen during the hypersensitive response (HR). It is also found in the cells challenged by necrotrophic pathogens (they are called necrotrophic because

they kill host cells to derive nutrients). However, in the case of the HR, necrotic features are often accompanied by the features of vacuolar cell death (see below). Cytological hallmarks

that distinguish plant necrosis from vacuolar cell death include mitochondrial swelling, the absence of the growing lytic vacuoles and an early rupture of the plasma membrane leading to

shrinkage of the protoplast (Table 1; Figure 2).9, 19, 32, 33 Because there are no lytic vacuoles that clear the cytoplasm during necrosis, the corpses of necrotic cells remain largely

unprocessed. A shrunken protoplast is one of the most easily detected features of plant necrotic cells (Figure 2). Time-course analysis of animal necrosis has revealed that the initial gain

in cell volume (swelling) as a result of ion pump failure is followed by cell shrinkage.30 Plant cells have a cell wall that should counteract swelling of the protoplast at early stages of

necrosis, which would therefore escape detection.32 However, an early loss of plasma membrane integrity can result in readily detectable protoplast shrinkage. Necrosis is typically an acute

cell death response that develops rapidly and takes from several minutes (toxic treatments) to up to a day, as seen in the HR. A recommended approach to diagnose plant necrosis is by

combining EM analysis with the assessment of mitochondrial dysfunction (MMP and decreased levels of both oxygen consumption and ATP production) and both ROS and RNS accumulation (Table 2).

MIXED AND ATYPICAL MODALITIES OF PLANT CELL DEATH HR WITH SOME FEATURES OF VACUOLAR CELL DEATH It has been long known that a programmed, localised cell death connected with the HR occurs at

the site of successful recognition of biotrophic pathogens. Whether this cell death is the cause of restricted pathogen replication or a consequence thereof has been debated for decades.34

The nature of the HR cell death with respect to its morphology has also been debated.35, 36, 37, 38, 39 Most recently, HR cell death and pathogen replication restriction have been de-coupled

by manipulation of metacaspase expression, showing that, for at least the pathogens tested, the elimination of the host cell death response does not lead to pathogen proliferation.40 HR

cell death usually exhibits all characteristics of plant cell necrosis (Tables 1 and 2). However, HR cell death is at the same time often accompanied by the growth of lytic vacuoles and

tonoplast rupture, which can require VPE from the vacuole in some cases.10, 41 In addition, increased autophagic activity before HR cell death is apparently controlled by _ATG_ genes,42

although the precise role of autophagy may differ depending on the particular HR cell death pathway being studied.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.11 SHRUNKEN

PROTOPLAST AND INTACT PLASMA MEMBRANE DURING VICTORIN-INDUCED CELL DEATH A particular cell death, evoked by the fungal toxin victorin, is important because it has evolved to use the host HR

as a means to kill cells, which are then ‘digested’ by the necrotrophic pathogen. Furthermore, similar to classic pathogen-induced HR, victorin sensitivity is dependent on an NB-LRR immune

receptor.46 Although victorin-induced cell death in oat plants exhibits hallmarks of necrosis such as protoplast shrinkage and MMP, the shrunken protoplast is surrounded by an intact plasma

membrane and the tonoplast retains its integrity.47 This suggests that initiation of the HR-related cell death can sometimes occur without the loss of membrane integrity.48 MIXTURE OF

VACUOLAR AND NECROTIC HALLMARKS DURING SELF-INCOMPATIBILITY RESPONSE During self-incompatibility (SI) response in _Papaver_, an incompatible pollen tube is stopped by interactions with the

pistil S-determinant that trigger a network of signalling events that converge to mediate PCD.49 SI cell death exhibits some characteristics of vacuolar cell death, including alterations to

the actin cytoskeleton, organelle engulfment and loss of vacuolar integrity. SI also has features of necrosis including swelling of the mitochondria and increase in [Ca2+]cyt.49, 50 A LONG

TIME GAP BETWEEN CELL DEATH AND CORPSE PROCESSING IN CEREAL STARCHY ENDOSPERM The cereal endosperm consists of the starchy endosperm surrounded by the aleurone cell layer. Cells of the

starchy endosperm accumulate storage reserves and die during seed maturation, but their corpses remain unprocessed until germination. Upon seed germination, aleurone cells secrete hydrolytic

enzymes that break down and mobilise the reserves accumulated in the dead starchy endosperm.51, 52 RECOMMENDATIONS TO AUTHORS, REVIEWERS AND EDITORS OF SCIENTIFIC JOURNALS Arbitrary and

sometimes contradictory usage of terminology has been a problem in the field of plant cell death research. Here we have grouped together morphological characteristics that distinguish two

major classes of cell death occurring in plants (Table 1). On the basis of this simplistic grouping, we suggest that terms ‘vacuolar cell death’ and ‘necrotic cell death’ (or ‘necrosis’) are

used when referring to corresponding classes of cell death in plants. Because the HR cell death with autolytic features, victorin-induced cell death, and both starchy endosperm and SI cell

death do not neatly fall into these two categories, we suggest that they are left as separate cell death modalities. The present classification is of course not static, but will be subjected

to further revisions, especially when specific biochemical pathways and molecular identity of mediators for plant PCD are better defined. We recommend that plant cell death researchers

abandon terms such as ‘apoptosis’ or ‘apoptotic-like’. We think such terminology is incorrect and misleading, because the features often cited are also found in other types of PCD, whereas

the _bona fide_ cytological characteristics of apoptosis (formation of apoptotic bodies and phagocytosis) are absent in plants. Adequate choices of analytical methods are required to

correctly diagnose a type of plant cell death (Table 2). Being a classic, cytological method, EM analysis provides excellent descriptive data on the changes in the dying cell for the initial

classification of the particular morphotype. We encourage the use of EM in showing the temporal details of the cell death under study, such as the structure of organelles, formation of

autophagosome-like structures, nuclear events and early detachment of plasma membrane from the cell wall (beginning of protoplast shrinkage). We would furthermore advise that experiments

with protoplasts are not used in isolation, but are supported by tests having a direct relationship to the physiologically relevant cell death in the model system. Several of the

recommendations formulated in the classification of animal cell death1 are also relevant to studies of plant cell death. For example, the term ‘dead cell’ should only be used for cells that

are shown to be dead by specific staining, such as fluorescein diacetate or Evan's blue. We thus encourage the use of quantification of cell death along with the necessary statistical

treatments to show significance for the reported data. CONCLUSION We recognise two major classes of cell death occurring in plant biology: (i) vacuolar cell death and (ii) necrotic cell

death. Vacuolar cell death occurs during plant tissue and organ formation and elimination, although necrosis is typically found under abiotic stress, some forms of the HR-related cell death

and cell death induced by necrotrophic pathogens. A few examples of cell death cannot be ascribed to either major class and therefore classified as separate modalities. This category

includes HR cell death with autolytic features and victorin-induced cell death, as well as cell death occurring in starchy cereal endosperm and during SI response. Further studies using

tools of genetics, biochemistry and cell biology are required to understand molecular mechanisms underlying variability of plant cell death morphology. ABBREVIATIONS * GFP: green fluorescent

protein * EM: electron microscopy * IF microscopy: immunofluorescent microscopy * HR: hypersensitive response * JC-1: JC-1 mitochondrial membrane potential detection kit based on

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INFORMATION AUTHORS AND AFFILIATIONS * Department of Plant Sciences, Mann Laboratory, University of California, Davis, 95616, CA, USA W G van Doorn * Department of Horticulture, Virginia

Polytechnic Institute and State University, Blacksburg, 24061, VA, USA E P Beers * Department of Biology and Carolina Center of Genome Science, University of North Carolina, Chapel Hill,

27599, NC, USA J L Dangl * School of Biosciences, College of Life and Environmental and Life Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK, V E Franklin-Tong *

Faculty of Life Sciences, University of Manchester, Manchester, M13 9PT, UK P Gallois * Department of Biological Science, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto

606-8502, Japan, I Hara-Nishimura * Departments of Biology and Pharmacology, University of North Carolina, Chapel Hill, 27599, NC, USA A M Jones * Department of Environmental Science and

Technology, Institute for Environmental Science and Technology, Saitama University, Saitama, 338-8570, Japan M Kawai-Yamada * Department of Plant Biology and Pathology, Rutgers the State

University of New Jersey, 59 Dudley Road, New Brunswick, 08901, NJ, USA E Lam * Department of Biology, University of Copenhagen, Ole Maaloes Vej 5, 220 Copenhagen, Denmark, J Mundy & M

Petersen * Aberystwyth University, Institute of Biological, Environmental and Rural Sciences, Aberystwyth, SY23 3DA, Wales, UK L A J Mur * The Integrative Cell Biology Laboratory, School of

Biological and Biomedical Sciences, University of Durham, South Road, DH1 3LE, Durham, UK A Smertenko * Plant Pathology Programme, Scottish Crop Research Institute, Invergowrie, Dundee DD2

5DA, UK, M Taliansky * VIB Department of Plant Systems Biology and Department of Plant Biotechnology and Genetics, University of Ghent, Technologiepark 927, Ghent 9052, Belgium, F Van

Breusegem * Department of Botany and Plant Pathology, Center for Genome Research and Biocomputing, Oregon State University, Corvallis, 97330, OR, USA T Wolpert * Horticultural Supply Chains,

Droevendaalsesteeg 1, and Food and Biobased Research, Bornse Weilanden 9, Wageningen University and Research Center, Wageningen, 6708, The Netherlands E Woltering * Division of Toxicology,

Institute of Environmental Medicine, Karolinska Institutet, Box 210, Stockholm171 77, Sweden, B Zhivotovsky * Department of Plant Biology and Forest Genetics, Uppsala BioCentre, Swedish

University of Agricultural Sciences, Box 7080, Uppsala 75007, Sweden, P V Bozhkov Authors * W G van Doorn View author publications You can also search for this author inPubMed Google Scholar

* E P Beers View author publications You can also search for this author inPubMed Google Scholar * J L Dangl View author publications You can also search for this author inPubMed Google

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COMPETING INTERESTS The authors declare no conflict of interest. ADDITIONAL INFORMATION Edited by V De Laurenzi RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS

ARTICLE van Doorn, W., Beers, E., Dangl, J. _et al._ Morphological classification of plant cell deaths. _Cell Death Differ_ 18, 1241–1246 (2011). https://doi.org/10.1038/cdd.2011.36 Download

citation * Received: 09 February 2011 * Accepted: 07 March 2011 * Published: 15 April 2011 * Issue Date: August 2011 * DOI: https://doi.org/10.1038/cdd.2011.36 SHARE THIS ARTICLE Anyone you

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Springer Nature SharedIt content-sharing initiative KEYWORDS * apoptosis * autophagy * cell wall * hypersensitive response * necrosis * vacuolar cell death