Johan Auwerx / Ecole polytechnique fédérale de Lausanne
Mitochondrial function is controlled by two separate genomes. This feature makes mitochondria prone to proteotoxic stress in case a stoichiometric imbalance occurs in protein complexes that perform oxidative phosphorylation (OXPHOS), which consist of both nuclear- and mitochondrial-encoded proteins. Such a proteotoxic stress is known to induce the mitochondrial unfolded protein response (UPRmt) in animals. It is unknown whether UPRmt occurs in plants. Here, we found that mitochondrial proteotoxic stress activated a plant-specific UPRmt and elongated plant life cycle. The retrograde signal is initiated by a fast oxidative burst, resulting in MPK6 activation, culminating in a systemic hormone response mainly reliant on ethylene signaling. This will activate an anterograde response that aims to repair mitochondrial translation and protein folding, which will ultimately compensate for the decreased level of OXPHOS components. Our data not only highlight the universal nature of key features of mitonuclear stress signaling pathways, but also indicate specific effectors (mitokines vs. phytohormones) and transcriptional circuits (ATF4/5 vs. ERFs) that are divergent between the plant and animal kingdoms. In summary, our study ascertains that the network of mitochondrial protein quality control pathways is conserved in plants and that hormone signaling is an essential mediator that regulates mitochondrial proteostasis.