Systems Phytohormone Responses to Mitochondrial Proteotoxic Stress

Abstract

Mitochondrial function is controlled by two separate genomes. This feature makes mitochondria prone to proteotoxic stress when a stoichiometric imbalance occurs in the protein complexes that perform oxidative phosphorylation, which consist of both nuclear- and mitochondrial-encoded proteins. Such a proteotoxic stress is known to induce the mitochondrial unfolded protein response (UPR^mt) in animals. It is unknown whether UPR^mt occurs in plants. Here, we induced a mitonuclear protein imbalance in Arabidopsis through chemical or genetic interference. Mitochondrial proteotoxic stress activated a plant-specific UPR^mt and impaired plant growth and development. The plant UPR^mt pathway is triggered by a transient oxidative burst, activating MAPK and hormonal (involving ethylene and auxin) signaling, which are all geared to repair proteostasis. This also establishes phytohormones as bona fide plant mitokines. Our data ascertain that mitochondrial protein quality control pathways, such as the UPR^mt, are conserved in plants and that hormone signaling is an essential mediator that regulates mitochondrial proteostasis.

Keywords: MAPK; ethylene; mitochondrial proteostasis; mitochondrial ribosomal protein; mitochondrial translation; mitochondrial unfolded protein response; mitochondrion; mitokine; phytohormone.