Morphological classification of plant cell deaths

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. 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.

Figure 1

Vacuolar cell death. Electron micrographs of programmed cell death (PCD) in the Norway spruce embryo-suspensor cells (top panels) and Arabidopsis tracheary elements (bottom panels). cw, cell wall; lv, lytic vacuole; n, nucleus; scw, secondary cell wall; t, tonoplast. Scale bars, 5 μm (embryo suspensor) and 500 nm (tracheary elements). Pictures of Norway spruce embryo-suspensor cells were kindly provided by Dr. Lada Filonova and Dr. Elena Minina (Swedish University of Agricultural Sciences, Uppsala, Sweden) and those of Arabidopsis tracheary elements by Dr. Utku Avci (University of Georgia, Complex Carbohydrate Research Center, Athens, GA, USA)

Figure 2

Necrotic cell death. Electron micrographs of Yariv reagent-induced death in the Arabidopsis cell culture (top panels) and ozone-induced death of the palisade cells in bean plants (bottom panels). Asterisks denote detachment of plasma membrane form the cell wall at early stage of cell death. c, chloroplast; cw, cell wall; pm, plasma membrane; t, tonoplast; v, vacuole. Scale bars, 2 μm. Pictures of Yariv reagent-induced cell death were kindly provided by Dr. Allan Showalter (Ohio University, Athens, OH, USA) and reproduced with permission from Gao and Showalter. Pictures of ozone-induced cell death were kindly provided by Dr. Franco Faoro (University of Milan, Milan, Italy)