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The transcription factor ANAC017 is a key regulator of mitochondrial proteotoxic stress responses in plants

Kacprzak, Sylwia M. LU ; Dahlqvist, Anton and Van Aken, Olivier LU (2020) In Philosophical Transactions of the Royal Society B: Biological Sciences 375(1801).
Abstract

Impaired mitochondrial translation or reduced mitochondrial protein import can lead to imbalances in mitochondrial protein composition. Such mitochondrial proteotoxic stresses can trigger a nuclear transcriptional response commonly described as the mitochondrial unfolded protein response (UPRmt). Despite extensive studies of UPRmt pathways in animal and fungal systems, very little is known about how the UPRmt is regulated in plants. Through comparison of Arabidopsis thaliana whole-genome transcriptome data, it was found that most genes induced by mitochondrial ribosome inhibitor doxycycline are also induced by Complex III inhibitor antimycin A. We demonstrate that transcriptional responses to a wide... (More)

Impaired mitochondrial translation or reduced mitochondrial protein import can lead to imbalances in mitochondrial protein composition. Such mitochondrial proteotoxic stresses can trigger a nuclear transcriptional response commonly described as the mitochondrial unfolded protein response (UPRmt). Despite extensive studies of UPRmt pathways in animal and fungal systems, very little is known about how the UPRmt is regulated in plants. Through comparison of Arabidopsis thaliana whole-genome transcriptome data, it was found that most genes induced by mitochondrial ribosome inhibitor doxycycline are also induced by Complex III inhibitor antimycin A. We demonstrate that transcriptional responses to a wide range of mitochondrial proteotoxic stress-triggers are regulated by the transcription factor ANAC017, which was shown to reside in the endoplasmic reticulum (ER). By contrast, no consistent evidence was found for genes that are specifically induced by doxycycline but not antimycin A. Furthermore, ANAC017 gain- and loss-of-function mutants showed marked resistance or susceptibility, respectively, to mitochondrial stress-inducing treatments, demonstrating the physiological importance of ANAC017 during mitochondrial proteotoxic stress. Finally, it was shown that ethylene signalling promotes mitochondria-to-nucleus signalling, most likely independently of ANAC017. Overall, this study shows that in plants, the UPRmt is largely overlapping with, and perhaps identical to, ‘classical’ mitochondrial retrograde signalling, and is mediated by ER-anchored transcription factor ANAC017. This article is part of the theme issue ‘Retrograde signalling from endosymbiotic organelles’.

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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Mitochondria, Retrograde signalling, Unfolded protein response, UPR
in
Philosophical Transactions of the Royal Society B: Biological Sciences
volume
375
issue
1801
article number
20190411
publisher
Royal Society
external identifiers
  • pmid:32362262
  • scopus:85085099770
ISSN
0962-8436
DOI
10.1098/rstb.2019.0411
language
English
LU publication?
yes
id
203f6b92-393f-4e2e-8db7-1937149d469b
date added to LUP
2020-06-12 13:00:14
date last changed
2020-07-08 05:17:05
@article{203f6b92-393f-4e2e-8db7-1937149d469b,
  abstract     = {<p>Impaired mitochondrial translation or reduced mitochondrial protein import can lead to imbalances in mitochondrial protein composition. Such mitochondrial proteotoxic stresses can trigger a nuclear transcriptional response commonly described as the mitochondrial unfolded protein response (UPR<sup>mt</sup>). Despite extensive studies of UPR<sup>mt</sup> pathways in animal and fungal systems, very little is known about how the UPR<sup>mt</sup> is regulated in plants. Through comparison of Arabidopsis thaliana whole-genome transcriptome data, it was found that most genes induced by mitochondrial ribosome inhibitor doxycycline are also induced by Complex III inhibitor antimycin A. We demonstrate that transcriptional responses to a wide range of mitochondrial proteotoxic stress-triggers are regulated by the transcription factor ANAC017, which was shown to reside in the endoplasmic reticulum (ER). By contrast, no consistent evidence was found for genes that are specifically induced by doxycycline but not antimycin A. Furthermore, ANAC017 gain- and loss-of-function mutants showed marked resistance or susceptibility, respectively, to mitochondrial stress-inducing treatments, demonstrating the physiological importance of ANAC017 during mitochondrial proteotoxic stress. Finally, it was shown that ethylene signalling promotes mitochondria-to-nucleus signalling, most likely independently of ANAC017. Overall, this study shows that in plants, the UPR<sup>mt</sup> is largely overlapping with, and perhaps identical to, ‘classical’ mitochondrial retrograde signalling, and is mediated by ER-anchored transcription factor ANAC017. This article is part of the theme issue ‘Retrograde signalling from endosymbiotic organelles’.</p>},
  author       = {Kacprzak, Sylwia M. and Dahlqvist, Anton and Van Aken, Olivier},
  issn         = {0962-8436},
  language     = {eng},
  number       = {1801},
  publisher    = {Royal Society},
  series       = {Philosophical Transactions of the Royal Society B: Biological Sciences},
  title        = {The transcription factor ANAC017 is a key regulator of mitochondrial proteotoxic stress responses in plants},
  url          = {http://dx.doi.org/10.1098/rstb.2019.0411},
  doi          = {10.1098/rstb.2019.0411},
  volume       = {375},
  year         = {2020},
}