Is the maintenance of homeostatic mitochondrial signaling during stress a physiological role for alternative oxidase?

Abstract

All plants maintain a non-energy-conserving pathway of mitochondrial electron transport referred to as alternative oxidase (AOX) respiration. Here, we briefly review some of the most prevailing themes for the metabolic and physiological roles of this respiratory pathway. Many of these themes relate to the potential of AOX to provide metabolic homeostasis in response to fluctuating cellular conditions, such as is often seen during stress. We then review reverse genetic experiments that have been used to test these hypotheses. To date, such experiments have been limited to just two dicot species and have only targeted one member (a stress-induced member) of the AOX multigene family. Nonetheless, the experiments to date strongly reinforce the idea that AOX respiration is of particular importance during abiotic and biotic stress. Finally, we propose that another core role of AOX may be to modulate the strength of a stress-signaling pathway from the mitochondrion that controls cellular responses to stress. In this way, AOX could be acting to provide a degree of signaling homeostasis from the mitochondrion. This hypothesis may provide explanation for some of the disparate results seen in reverse genetic experiments regarding the impact of AOX on the reactive oxygen network and oxidative damage.

Decreasing Electron Flux through the Cytochrome and/or Alternative Respiratory Pathways Triggers Common and Distinct Cellular Responses Dependent on Growth Conditions

“…Investigations with a variety of abiotic or biotic challenges revealed that AOX acts as a survival protein (Vanlerberghe et al, 2009), in that it allows plants to survive and grow better compared with plants that have reduced amounts of AOX. More detailed studies on the role of AOX in tobacco and Arabidopsis (Arabidopsis thaliana) showed that it not only suppresses the production of ROS (see studies outlined above) but also, by its activity, it mediates or determines signals coming from mitochondria (Arnholdt-Schmitt et al, 2006;Clifton et al, 2006;Vanlerberghe et al, 2009).…”

Extending Cassava Root Shelf Life via Reduction of Reactive Oxygen Species Production

“…Hansen et al (2002) have shown that the plant growth rate is proportional to the rate of respiration and the efficiency by which it is coupled to phosphorylation. Control of AOX expression could provide a means by which respiration is adjusted to the energetic needs of cellular activities (Vanlerberghe et al, 2009). By modulating energy yield (ATP production and NADH consumption), AOX may also play a role in optimizing the rate of high-energyconsuming processes (Vanlerberghe et al, 2009).…”

“…Control of AOX expression could provide a means by which respiration is adjusted to the energetic needs of cellular activities (Vanlerberghe et al, 2009). By modulating energy yield (ATP production and NADH consumption), AOX may also play a role in optimizing the rate of high-energyconsuming processes (Vanlerberghe et al, 2009). Since overexpression of AOX has been linked to stress tolerance, it will be necessary to investigate the changes in yield under different stress conditions.…”

How do plants make mitochondria?

“…It has become clear that mitochondria are not merely passive player(s) that respond to changes in the cellular environment, but rather that they can trigger these changes Van Aken et al 2009;Vanlerberghe et al 2009). While the concept of mitochondrial-to-nuclear signaling has been studied from the point of view of regulation of mitochondrial components, the identity of the molecular components that sense mitochondrial function and relay these signals to the nucleus remains unknown.…”