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

Autor: Florentine Ballhaus, Peter V. Bozhkov, Andrei Smertenko, Vladimir Gogvadze, Adrian N. Dauphinee, Elena A. Minina
Rok vydání: 2020
Předmět:
0106 biological sciences
Programmed cell death
Necrosis
Physiology
QH301-705.5
Phagocytosis
Cell
Regulated cell death
Apoptosis
Plant Science
Stress
01 natural sciences
General Biochemistry
Genetics and Molecular Biology

03 medical and health sciences
Structural Biology
Plant Cells
medicine
Ferroptosis
Animals
Fragmentation (cell biology)
Biology (General)
Ecology
Evolution
Behavior and Systematics

Caspase
030304 developmental biology
2. Zero hunger
0303 health sciences
biology
Cell Death
Botany
Cell Biology
Plants
Cell biology
medicine.anatomical_structure
Heat shock
Apoptosis-like programmed cell death
Caspases
biology.protein
Plasma membrane integrity
Protoplast shrinkage
medicine.symptom
General Agricultural and Biological Sciences
Mitochondrial dysfunction
Intracellular
Developmental Biology
Biotechnology
010606 plant biology & botany
Research Article
Zdroj: BMC Biology
BMC Biology, Vol 19, Iss 1, Pp 1-17 (2021)
ISSN: 1741-7007
Popis: BackgroundAnimals 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.ResultsHere, 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.ConclusionsWe 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.
Databáze: OpenAIRE