mTERF18 and ATAD3 are required for mitochondrial nucleoid structure and their disruption confers heat tolerance in Arabidopsis thaliana

Mitochondria play critical roles in generating ATP through oxidative phosphorylation (OXPHOS) and produce both damaging and signaling reactive oxygen species (ROS). They have reduced genomes that encode essential subunits of the OXPHOS machinery. Mitochondrial Transcription tERmination Factor-related (mTERF) proteins are involved in organelle gene expression, interacting with organellar DNA or RNA. We previously found that mutations in Arabidopsis thaliana mTERF18/SHOT1 enable plants to better tolerate heat and oxidative stresses, presumably due to low ROS production and reduced oxidative damage. Here we discover that shot1 mutants have greatly reduced OXPHOS complexes I and IV and reveal that suppressor of hot1-4 1 (SHOT1) binds DNA and localizes to mitochondrial nucleoids, which are disrupted in shot1. Furthermore, three homologues of animal ATPase family AAA domain-containing protein 3 (ATAD3), which is involved in mitochondrial nucleoid organization, were identified as SHOT1-interacting proteins. Importantly, disrupting ATAD3 function disrupts nucleoids, reduces accumulation of complex I, and enhances heat tolerance, as is seen in shot1 mutants. Our data link nucleoid organization to OXPHOS biogenesis and suggest that the common defects in shot1 mutants and ATAD3-disrupted plants lead to critical changes in mitochondrial metabolism and signaling that result in plant heat tolerance.