Apoptosis is not conserved in plants as revealed by critical examination of a model for plant apoptosis-like cell death

Abstract

Background Animals and plants diverged over one billion years ago and evolved unique mechanisms for many cellular processes, including cell death. One of the most well-studied cell death programmes in animals, apoptosis, involves gradual cell dismantling and engulfment of cellular fragments, apoptotic bodies, through phagocytosis. However, rigid cell walls prevent plant cell fragmentation and thus apoptosis is not applicable for executing cell death in plants. Furthermore, plants are devoid of the key components of apoptotic machinery, including phagocytosis as well as caspases and Bcl-2 family proteins. Nevertheless, the concept of plant “apoptosis-like programmed cell death” (AL-PCD) is widespread. This is largely due to superficial morphological resemblances between plant cell death and apoptosis, and in particular between protoplast shrinkage in plant cells killed by various stimuli and animal cell volume decrease preceding fragmentation into apoptotic bodies. Results Here, we provide a comprehensive spatio-temporal analysis of cytological and biochemical events occurring in plant cells subjected to heat shock at 40–55 °C and 85 °C, the experimental conditions typically used to trigger AL-PCD and necrotic cell death, respectively. We show that cell death under both conditions was not accompanied by membrane blebbing or formation of apoptotic bodies, as would be expected during apoptosis. Instead, we observed instant and irreversible permeabilization of the plasma membrane and ATP depletion. These processes did not depend on mitochondrial functionality or the presence of Ca2+ and could not be prevented by an inhibitor of ferroptosis. We further reveal that the lack of protoplast shrinkage at 85 °C, the only striking morphological difference between cell deaths induced by 40–55 °C or 85 °C heat shock, is a consequence of the fixative effect of the high temperature on intracellular contents. Conclusions We conclude that heat shock-induced cell death is an energy-independent process best matching definition of necrosis. Although the initial steps of this necrotic cell death could be genetically regulated, classifying it as apoptosis or AL-PCD is a terminological misnomer. Our work supports the viewpoint that apoptosis is not conserved across animal and plant kingdoms and demonstrates the importance of focusing on plant-specific aspects of cell death pathways.

Activating plant immunity: the hidden dance of intracellular Ca2+ stores

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Cell death as a defense strategy against pathogens in plants and animals

“…Apoptosis is an immunologically silent form of cell death in which gradual dismantling of the cell content leads to morphological features such as cytoplasmic shrinkage, chromatin condensation, and DNA fragmentation [ 30 ]. As opposed to other cell death programs, PM integrity is retained throughout the cell death process.…”

The role of Atg16 in autophagy, anthocyanin biosynthesis, and programmed cell death in leaves of the lace plant (Aponogeton madagascariensis)

“…Common examples of developmental PCD in plants used to achieve higher tissue organization include aerenchyma formation and xylem differentiation, suspensor and tapetum cell deletion, the dismantling of rapidly growing root tip cells, and organ senescence [ 4 – 10 ]. The molecular pathways that control PCD in animal models are relatively well identified compared to those involved in plant developmental PCD which is less understood [ 5 , 11 , 12 ].…”