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

Minina, Elena A. and Dauphinee, Adrian and Ballhaus, Florentine and Gogvadze, Vladimir and Smertenko, Andrei P. and Bozhkov, Peter (2021). Apoptosis is not conserved in plants as revealed by critical examination of a model for plant apoptosis-like cell death. BMC Biology. 19 , 100
[Research article]

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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 degrees C and 85 degrees 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 degrees C, the only striking morphological difference between cell deaths induced by 40-55 degrees C or 85 degrees 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.

Authors/Creators:Minina, Elena A. and Dauphinee, Adrian and Ballhaus, Florentine and Gogvadze, Vladimir and Smertenko, Andrei P. and Bozhkov, Peter
Title:Apoptosis is not conserved in plants as revealed by critical examination of a model for plant apoptosis-like cell death
Series Name/Journal:BMC Biology
Year of publishing :2021
Volume:19
Article number:100
Number of Pages:17
Publisher:BMC
ISSN:1741-7007
Language:English
Publication Type:Research article
Article category:Scientific peer reviewed
Version:Published version
Copyright:Creative Commons: Attribution 4.0
Full Text Status:Public
Subjects:(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Botany
Keywords:Apoptosis, Apoptosis-like programmed cell death, Ferroptosis, Heat shock, Mitochondrial dysfunction, Necrosis, Plants, Plasma membrane integrity, Protoplast shrinkage, Regulated cell death, Stress
URN:NBN:urn:nbn:se:slu:epsilon-p-111870
Permanent URL:
http://urn.kb.se/resolve?urn=urn:nbn:se:slu:epsilon-p-111870
Additional ID:
Type of IDID
DOI10.1186/s12915-021-01018-z
Web of Science (WoS)000649729300001
ID Code:23721
Faculty:NJ - Fakulteten för naturresurser och jordbruksvetenskap
Department:(NL, NJ) > Department of Molecular Sciences
Deposited By: SLUpub Connector
Deposited On:20 May 2021 11:44
Metadata Last Modified:20 May 2021 11:51

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