Skip to main content

Lund University Publications

LUND UNIVERSITY LIBRARIES

Mitochondria-derived reactive oxygen species are the likely primary trigger of mitochondrial retrograde signaling in Arabidopsis

Khan, Kasim LU ; Tran, Huy Cuong LU orcid ; Mansuroglu, Berivan LU ; Önsell, Pinar ; Buratti, Stefano ; Schwarzländer, Markus ; Costa, Alex ; Rasmusson, Allan G LU orcid and Van Aken, Olivier LU (2024) In Current biology : CB 34(2). p.4-342
Abstract

Besides their central function in respiration, plant mitochondria play a crucial role in maintaining cellular homeostasis during stress by providing "retrograde" feedback to the nucleus. Despite the growing understanding of this signaling network, the nature of the signals that initiate mitochondrial retrograde regulation (MRR) in plants remains unknown. Here, we investigated the dynamics and causative relationship of a wide range of mitochondria-related parameters for MRR, using a combination of Arabidopsis fluorescent protein biosensor lines, in vitro assays, and genetic and pharmacological approaches. We show that previously linked physiological parameters, including changes in cytosolic ATP, NADH/NAD+ ratio, cytosolic reactive... (More)

Besides their central function in respiration, plant mitochondria play a crucial role in maintaining cellular homeostasis during stress by providing "retrograde" feedback to the nucleus. Despite the growing understanding of this signaling network, the nature of the signals that initiate mitochondrial retrograde regulation (MRR) in plants remains unknown. Here, we investigated the dynamics and causative relationship of a wide range of mitochondria-related parameters for MRR, using a combination of Arabidopsis fluorescent protein biosensor lines, in vitro assays, and genetic and pharmacological approaches. We show that previously linked physiological parameters, including changes in cytosolic ATP, NADH/NAD+ ratio, cytosolic reactive oxygen species (ROS), pH, free Ca2+, and mitochondrial membrane potential, may often be correlated with-but are not the primary drivers of-MRR induction in plants. However, we demonstrate that the induced production of mitochondrial ROS is the likely primary trigger for MRR induction in Arabidopsis. Furthermore, we demonstrate that mitochondrial ROS-mediated signaling uses the ER-localized ANAC017-pathway to induce MRR response. Finally, our data suggest that mitochondrially generated ROS can induce MRR without substantially leaking into other cellular compartments such as the cytosol or ER lumen, as previously proposed. Overall, our results offer compelling evidence that mitochondrial ROS elevation is the likely trigger of MRR.

(Less)
Please use this url to cite or link to this publication:
author
; ; ; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Arabidopsis/genetics, Reactive Oxygen Species/metabolism, Arabidopsis Proteins/metabolism, Cytosol/metabolism, Mitochondria/metabolism, Transcription Factors/metabolism
in
Current biology : CB
volume
34
issue
2
pages
4 - 342
publisher
Elsevier
external identifiers
  • pmid:38176418
  • scopus:85182927448
ISSN
1879-0445
DOI
10.1016/j.cub.2023.12.005
language
English
LU publication?
yes
additional info
Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.
id
f5f8c911-c6f1-4b69-8fdc-923d652c83f0
date added to LUP
2025-12-01 14:30:39
date last changed
2025-12-30 06:35:51
@article{f5f8c911-c6f1-4b69-8fdc-923d652c83f0,
  abstract     = {{<p>Besides their central function in respiration, plant mitochondria play a crucial role in maintaining cellular homeostasis during stress by providing "retrograde" feedback to the nucleus. Despite the growing understanding of this signaling network, the nature of the signals that initiate mitochondrial retrograde regulation (MRR) in plants remains unknown. Here, we investigated the dynamics and causative relationship of a wide range of mitochondria-related parameters for MRR, using a combination of Arabidopsis fluorescent protein biosensor lines, in vitro assays, and genetic and pharmacological approaches. We show that previously linked physiological parameters, including changes in cytosolic ATP, NADH/NAD+ ratio, cytosolic reactive oxygen species (ROS), pH, free Ca2+, and mitochondrial membrane potential, may often be correlated with-but are not the primary drivers of-MRR induction in plants. However, we demonstrate that the induced production of mitochondrial ROS is the likely primary trigger for MRR induction in Arabidopsis. Furthermore, we demonstrate that mitochondrial ROS-mediated signaling uses the ER-localized ANAC017-pathway to induce MRR response. Finally, our data suggest that mitochondrially generated ROS can induce MRR without substantially leaking into other cellular compartments such as the cytosol or ER lumen, as previously proposed. Overall, our results offer compelling evidence that mitochondrial ROS elevation is the likely trigger of MRR.</p>}},
  author       = {{Khan, Kasim and Tran, Huy Cuong and Mansuroglu, Berivan and Önsell, Pinar and Buratti, Stefano and Schwarzländer, Markus and Costa, Alex and Rasmusson, Allan G and Van Aken, Olivier}},
  issn         = {{1879-0445}},
  keywords     = {{Arabidopsis/genetics; Reactive Oxygen Species/metabolism; Arabidopsis Proteins/metabolism; Cytosol/metabolism; Mitochondria/metabolism; Transcription Factors/metabolism}},
  language     = {{eng}},
  month        = {{01}},
  number       = {{2}},
  pages        = {{4--342}},
  publisher    = {{Elsevier}},
  series       = {{Current biology : CB}},
  title        = {{Mitochondria-derived reactive oxygen species are the likely primary trigger of mitochondrial retrograde signaling in Arabidopsis}},
  url          = {{http://dx.doi.org/10.1016/j.cub.2023.12.005}},
  doi          = {{10.1016/j.cub.2023.12.005}},
  volume       = {{34}},
  year         = {{2024}},
}