Interactions between mitochondrial electron transport, reactive oxygen species, and the susceptibility of Nicotiana tabacum cells to programmed cell death

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We investigated the impact of steady-state cellular reactive oxygen species (ROS) level on subsequent susceptibility to cell death induction by signaling molecules or respiratory inhibitors. We utilized Nicotiana tabacum L. (‘Petit Havana SR1’) suspension cell lines differing in steady-state ROS level owing to either genetic manipulation of the mitochondrial electron transport chain or manipulation of growth conditions. In either case, higher steady-state ROS level increased susceptibility to the signaling molecules salicylic acid and nitric oxide, suggesting that these molecules can engage a “steady-state ROS-primed cell death pathway”. We found that susceptibility to the complex III inhibitor antimycin A (AA) was also dependent upon steady-state ROS level and that this susceptibility was independent of that afforded by the inhibition of energy metabolism by AA. AA was unique in this respect, since susceptibility to two other electron transport chain inhibitors appeared strictly dependent upon their ability to inhibit energy metabolism. The results indicate that complex III may have a particular capacity to engage the steady-state ROS-primed cell death pathway (similarly to salicylic acid and nitric oxide) and may relate to the ability of this complex to generate superoxide. We also examined changes in cellular ROS post-treatment with the signaling molecules and respiratory inhibitors. In this case, the more susceptible cells (i.e., those that had experienced higher steady-state ROS levels) exhibited post-treatment declines in cellular ROS level, whereas the less susceptible cells were able to better maintain or increase their ROS post-treatment. This differential response may be an important determinant of cell fate.