Cytochrome c levels link mitochondrial function to plant growth and stress responses through changes in SnRK1 pathway activity

SUMMARY Energy is required for growth as well as for multiple cellular processes. During evolution, plants developed regulatory mechanisms to adapt energy consumption to metabolic reserves and cellular needs. Reduced growth is often observed under stress, leading to a growth‐stress trade‐off that governs plant performance under different conditions. In this work, we report that plants with reduced levels of the mitochondrial respiratory chain component cytochrome c (CYTc), required for electron transport coupled to oxidative phosphorylation and ATP production, show impaired growth and increased global expression of stress‐responsive genes, similar to those observed after inhibiting the respiratory chain or the mitochondrial ATP synthase. CYTc‐deficient plants also show activation of the SnRK1 pathway, which regulates growth, metabolism, and stress responses under carbon starvation conditions, even though their carbohydrate levels are not significantly different from wild‐type. Notably, loss‐of‐function of the gene encoding the SnRK1α1 subunit restores the growth of CYTc‐deficient plants, as well as autophagy, free amino acid and TOR pathway activity levels, which are affected in these plants. Moreover, increasing CYTc levels decreases SnRK1 pathway activation, reflected in reduced SnRK1α1 phosphorylation, with no changes in total SnRK1α1 protein levels. Under stress imposed by mannitol, the growth of CYTc‐deficient plants is relatively less affected than that of wild‐type plants, which is also related to the activation of the SnRK1 pathway. Our results indicate that SnRK1 function is affected by CYTc levels, thus providing a molecular link between mitochondrial function and plant growth under normal and stress conditions. Significance Statement Mitochondria are signalling hubs that integrate and transmit biological information to affect different cellular processes. We show that changes in the mitochondrial electron transport chain component cytochrome c influence growth and other plant characteristics under normal and stressful conditions through changes in the activation state of the carbon/energy sensor SnRK1, thus establishing a molecular link between mitochondria and plant growth, involved in adjusting plant performance according to the activity of these energy‐producing organelles.