The boundary of life and death: changes in mitochondrial and cytosolic proteomes associated with programmed cell death of Arabidopsis thaliana suspension culture cells

IntroductionDespite the critical role of programmed cell death (PCD) in plant development and defense responses, its regulation is not fully understood. It has been proposed that mitochondria may be important in the control of the early stages of plant PCD, but the details of this regulation are cur...

Full description

Bibliographic Details
Main Authors: Johanna Schwarze, James C. Carolan, Gavin S. Stewart, Paul F. McCabe, Joanna Kacprzyk
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-08-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1194866/full
_version_ 1797767074308685824
author Johanna Schwarze
James C. Carolan
Gavin S. Stewart
Paul F. McCabe
Joanna Kacprzyk
author_facet Johanna Schwarze
James C. Carolan
Gavin S. Stewart
Paul F. McCabe
Joanna Kacprzyk
author_sort Johanna Schwarze
collection DOAJ
description IntroductionDespite the critical role of programmed cell death (PCD) in plant development and defense responses, its regulation is not fully understood. It has been proposed that mitochondria may be important in the control of the early stages of plant PCD, but the details of this regulation are currently unknown. MethodsWe used Arabidopsis thaliana cell suspension culture, a model system that enables induction and precise monitoring of PCD rates, as well as chemical manipulation of this process to generate a quantitative profile of the alterations in mitochondrial and cytosolic proteomes associated with early stages of plant PCD induced by heat stress. The cells were subjected to PCD-inducing heat levels (10 min, 54°C), with/without the calcium channel inhibitor and PCD blocker LaCl3. The stress treatment was followed by separation of cytosolic and mitochondrial fractions and mass spectrometry-based proteome analysis. ResultsHeat stress induced rapid and extensive changes in protein abundance in both fractions, with release of mitochondrial proteins into the cytosol upon PCD induction. In our system, LaCl3 appeared to act downstream of cell death initiation signal, as it did not affect the release of mitochondrial proteins, but instead partially inhibited changes occurring in the cytosolic fraction, including upregulation of proteins with hydrolytic activity. DiscussionWe characterized changes in protein abundance and localization associated with the early stages of heat stress-induced PCD. Collectively, the generated data provide new insights into the regulation of cell death and survival decisions in plant cells.
first_indexed 2024-03-12T20:34:16Z
format Article
id doaj.art-6bf7d550f2ef473c966f61aeab7399da
institution Directory Open Access Journal
issn 1664-462X
language English
last_indexed 2024-03-12T20:34:16Z
publishDate 2023-08-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Plant Science
spelling doaj.art-6bf7d550f2ef473c966f61aeab7399da2023-08-01T15:48:47ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-08-011410.3389/fpls.2023.11948661194866The boundary of life and death: changes in mitochondrial and cytosolic proteomes associated with programmed cell death of Arabidopsis thaliana suspension culture cellsJohanna Schwarze0James C. Carolan1Gavin S. Stewart2Paul F. McCabe3Joanna Kacprzyk4School of Biology and Environmental Science, University College Dublin, Dublin, IrelandDepartment of Biology, Maynooth University, Maynooth, IrelandSchool of Biology and Environmental Science, University College Dublin, Dublin, IrelandSchool of Biology and Environmental Science, University College Dublin, Dublin, IrelandSchool of Biology and Environmental Science, University College Dublin, Dublin, IrelandIntroductionDespite the critical role of programmed cell death (PCD) in plant development and defense responses, its regulation is not fully understood. It has been proposed that mitochondria may be important in the control of the early stages of plant PCD, but the details of this regulation are currently unknown. MethodsWe used Arabidopsis thaliana cell suspension culture, a model system that enables induction and precise monitoring of PCD rates, as well as chemical manipulation of this process to generate a quantitative profile of the alterations in mitochondrial and cytosolic proteomes associated with early stages of plant PCD induced by heat stress. The cells were subjected to PCD-inducing heat levels (10 min, 54°C), with/without the calcium channel inhibitor and PCD blocker LaCl3. The stress treatment was followed by separation of cytosolic and mitochondrial fractions and mass spectrometry-based proteome analysis. ResultsHeat stress induced rapid and extensive changes in protein abundance in both fractions, with release of mitochondrial proteins into the cytosol upon PCD induction. In our system, LaCl3 appeared to act downstream of cell death initiation signal, as it did not affect the release of mitochondrial proteins, but instead partially inhibited changes occurring in the cytosolic fraction, including upregulation of proteins with hydrolytic activity. DiscussionWe characterized changes in protein abundance and localization associated with the early stages of heat stress-induced PCD. Collectively, the generated data provide new insights into the regulation of cell death and survival decisions in plant cells. https://www.frontiersin.org/articles/10.3389/fpls.2023.1194866/fullplant programmed cell deathmitochondriaproteomicsheat stresscytosol
spellingShingle Johanna Schwarze
James C. Carolan
Gavin S. Stewart
Paul F. McCabe
Joanna Kacprzyk
The boundary of life and death: changes in mitochondrial and cytosolic proteomes associated with programmed cell death of Arabidopsis thaliana suspension culture cells
Frontiers in Plant Science
plant programmed cell death
mitochondria
proteomics
heat stress
cytosol
title The boundary of life and death: changes in mitochondrial and cytosolic proteomes associated with programmed cell death of Arabidopsis thaliana suspension culture cells
title_full The boundary of life and death: changes in mitochondrial and cytosolic proteomes associated with programmed cell death of Arabidopsis thaliana suspension culture cells
title_fullStr The boundary of life and death: changes in mitochondrial and cytosolic proteomes associated with programmed cell death of Arabidopsis thaliana suspension culture cells
title_full_unstemmed The boundary of life and death: changes in mitochondrial and cytosolic proteomes associated with programmed cell death of Arabidopsis thaliana suspension culture cells
title_short The boundary of life and death: changes in mitochondrial and cytosolic proteomes associated with programmed cell death of Arabidopsis thaliana suspension culture cells
title_sort boundary of life and death changes in mitochondrial and cytosolic proteomes associated with programmed cell death of arabidopsis thaliana suspension culture cells
topic plant programmed cell death
mitochondria
proteomics
heat stress
cytosol
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1194866/full
work_keys_str_mv AT johannaschwarze theboundaryoflifeanddeathchangesinmitochondrialandcytosolicproteomesassociatedwithprogrammedcelldeathofarabidopsisthalianasuspensionculturecells
AT jamesccarolan theboundaryoflifeanddeathchangesinmitochondrialandcytosolicproteomesassociatedwithprogrammedcelldeathofarabidopsisthalianasuspensionculturecells
AT gavinsstewart theboundaryoflifeanddeathchangesinmitochondrialandcytosolicproteomesassociatedwithprogrammedcelldeathofarabidopsisthalianasuspensionculturecells
AT paulfmccabe theboundaryoflifeanddeathchangesinmitochondrialandcytosolicproteomesassociatedwithprogrammedcelldeathofarabidopsisthalianasuspensionculturecells
AT joannakacprzyk theboundaryoflifeanddeathchangesinmitochondrialandcytosolicproteomesassociatedwithprogrammedcelldeathofarabidopsisthalianasuspensionculturecells
AT johannaschwarze boundaryoflifeanddeathchangesinmitochondrialandcytosolicproteomesassociatedwithprogrammedcelldeathofarabidopsisthalianasuspensionculturecells
AT jamesccarolan boundaryoflifeanddeathchangesinmitochondrialandcytosolicproteomesassociatedwithprogrammedcelldeathofarabidopsisthalianasuspensionculturecells
AT gavinsstewart boundaryoflifeanddeathchangesinmitochondrialandcytosolicproteomesassociatedwithprogrammedcelldeathofarabidopsisthalianasuspensionculturecells
AT paulfmccabe boundaryoflifeanddeathchangesinmitochondrialandcytosolicproteomesassociatedwithprogrammedcelldeathofarabidopsisthalianasuspensionculturecells
AT joannakacprzyk boundaryoflifeanddeathchangesinmitochondrialandcytosolicproteomesassociatedwithprogrammedcelldeathofarabidopsisthalianasuspensionculturecells