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

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T1 - The transcription factor ANAC017 is a key regulator of mitochondrial proteotoxic stress responses in plants

AU - Kacprzak, Sylwia M.

AU - Dahlqvist, Anton

AU - Van Aken, Olivier

PY - 2020

Y1 - 2020

N2 - 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’.

AB - 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’.

KW - Mitochondria

KW - Retrograde signalling

KW - Unfolded protein response

KW - UPR

U2 - 10.1098/rstb.2019.0411

DO - 10.1098/rstb.2019.0411

M3 - Article

C2 - 32362262

AN - SCOPUS:85085099770

VL - 375

JO - Philosophical Transactions of the Royal Society B: Biological Sciences

JF - Philosophical Transactions of the Royal Society B: Biological Sciences

SN - 1471-2970

IS - 1801

M1 - 20190411

ER -