The transcription factor ANAC017 is a key regulator of mitochondrial proteotoxic stress responses in plants
(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’.
(Less)
- author
- Kacprzak, Sylwia M. LU ; Dahlqvist, Anton and Van Aken, Olivier LU
- organization
- publishing date
- 2020
- 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 Publishing
- 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
- 2024-09-04 22:57:13
@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}}, keywords = {{Mitochondria; Retrograde signalling; Unfolded protein response; UPR}}, language = {{eng}}, number = {{1801}}, publisher = {{Royal Society Publishing}}, 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}}, }