Loss of Mitochondrial ADP/ATP carrier 1 affects mitochondrial morphology and plant growth

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Abstract
Cellular energy homeostasis relies on the precise exchange of nucleotides across subcellular compartments. The transport of ADP and ATP is essential for maintaining cellular energy balance. Transporters of these molecules are abundant proteins in the mitochondrial membrane, mediating their exchange between the mitochondrial matrix and the cytosol. In this study, we investigated the function of ADP/ATP Carrier 1 (AAC1) in plants to understand whether its regulation and function are similar to those described in animal and yeast systems. Our results revealed that AAC1 specifically transports ADP and ATP, while aac1 mutants displayed lower O2 consumption without evident decreases in cytosolic ATP levels. However, total adenylate profiling revealed altered adenylate balance and reduced adenylate energy charge in aac1 roots, indicating that reduced AAC1 function perturbs energy homeostasis beyond changes in ATP content alone. AAC1 was also required for proper mitochondrial structure, as aac1 mutant mitochondria exhibited a less electron-dense matrix and occasional absence of cristae. Suppressing AAC1 expression in plants altered vegetative and reproductive growth, reducing leaf number and root elongation while increasing silique size and seed weight. These findings provide novel insight into the role of AAC1 in mitochondrial energy dynamics. Biochemical analyses show a high specificity of AAC1 for adenine nucleotides, facilitating ADP/ATP exchange driven by the mitochondrial membrane potential, while excluding monophosphates and divalent ATP complexes. By correlating these biochemical characteristics with impaired mitochondrial respiration, altered adenylate balance, ultrastructural defects, and altered energy allocation, our study highlights the broader physiological impacts of disrupted adenylate transport mediated by AAC1.