Nitric oxide suppresses the energy transduction of plant mitochondria

Abstract

Plant mitochondria are known to possess two respiratory electron transport pathways, i.e. the cytochrome and alternative pathways. The physiological function(s) of the alternative pathway are not fully understood. It has been proposed that the alternative pathway may play an important role in preventing oxidative damage induced by nitric oxide (NO). We have recently revealed that plant nitrate reductase (NR) is capable of converting nitrite to NO. By using the NR-catalyzed NO production system, we investigated in vitro effects of NO on the energy transduction system of mitochondria. When the alternative pathway was inhibited by n-propyl gallate, the addition of NR strongly suppressed respiratory O2 consumption driven by the cytochrome pathway. In contrast, the alternative pathway in the presence of antimycin A was not affected by NO. The extent of the steady-state membrane potential generated by respiratory electron transport rapidly declined in response to NO production. The addition of bovine hemoglobin, a quencher of NO, resulted in recovery of the membrane potential to the uninhibited level. Consistent with its inhibition of the membrane potential, NO produced by NR strongly suppressed ATP synthesis in mitochondria. These results provide substantial evidence to confirm that the plant alternative pathway is resistant to NO. We suggest that the alternative pathway could be required in photoinhibiting conditions where NR potentially overproduces NO.