Roles for Plant Mitochondrial Alternative Oxidase Under Normoxia, Hypoxia, and Reoxygenation Conditions
Citation
Jayawardhane, J., Cochrane, D.W., Vyas, P., Bykova, N.V., Vanlerberghe, G.C., Igamberdiev, A.U. (2020). Roles for Plant Mitochondrial Alternative Oxidase Under Normoxia, Hypoxia, and Reoxygenation Conditions. Frontiers in Plant Science, [online] 11 http://dx.doi.org/10.3389/fpls.2020.00566
Plain language summary
Plant mitochondrial electron transfer chain has branched pathways consisting of two distinct terminal oxidases resulting in different energy yields. The electron flow from lipid-soluble component ubiquinol to oxygen via the cytochrome c oxidase contributes to the synthesis of ATP, whereas the electron flow via alternative oxidase (AOX) is not coupled to ATP synthesis. This provides plant mitochondria means for high metabolic flexibility to maintain energy balance in response to changing demands imposed by internal and external factors, especially fluctuations in cellular oxygen concentration. In this study, researchers show that, despite its lower affinity for oxygen than cytochrome oxidase, AOX plays a beneficial role in low oxygen metabolism. The results show that in wild type, AOX knockdown and overexpression plants under different oxygen conditions, normal levels, oxygen deficiency and upon return to normal oxygen levels, AOX amount influences leaf carbon and energy metabolism. The study demonstrates that the role of AOX in the maintenance of respiratory carbon flow changes depending on the oxygen concentration. Under normal oxygen levels AOX prevents the mitochondrial generation of superoxide and nitric oxide (NO), thereby preventing lipid peroxidation and protein modification by NO. The analysis shows that AOX limits superoxide generation and lipid peroxidation but contributes to NO generation under the conditions of oxygen deficiency. The present study demonstrates that AOX is particularly important in preventing nitro-oxidative stress upon return to normal oxygen levels after the conditions of oxygen deficiency, thus contributing positively to the recovery of mitochondrial energy status following hypoxia.
Abstract
Alternative oxidase (AOX) is a non-energy conserving terminal oxidase in the plant mitochondrial electron transport chain (ETC) that has a lower affinity for oxygen than does cytochrome (cyt) oxidase. To investigate the role(s) of AOX under different oxygen conditions, wild-type (WT) Nicotiana tabacum plants were compared with AOX knockdown and overexpression plants under normoxia, hypoxia (near-anoxia), and during a reoxygenation period following hypoxia. Paradoxically, under all the conditions tested, the AOX amount across plant lines correlated positively with leaf energy status (ATP/ADP ratio). Under normoxia, AOX was important to maintain respiratory carbon flow, to prevent the mitochondrial generation of superoxide and nitric oxide (NO), to control lipid peroxidation and protein S-nitrosylation, and possibly to reduce the inhibition of cyt oxidase by NO. Under hypoxia, AOX was again important in preventing superoxide generation and lipid peroxidation, but now contributed positively to NO amount. This may indicate an ability of AOX to generate NO under hypoxia, similar to the nitrite reductase activity of cyt oxidase under hypoxia. Alternatively, it may indicate that AOX activity simply reduces the amount of superoxide scavenging of NO, by reducing the availability of superoxide. The amount of inactivation of mitochondrial aconitase during hypoxia was also dependent upon AOX amount, perhaps through its effects on NO amount, and this influenced carbon flow under hypoxia. Finally, AOX was particularly important in preventing nitro-oxidative stress during the reoxygenation period, thereby contributing positively to the recovery of energy status following hypoxia. Overall, the results suggest that AOX plays a beneficial role in low oxygen metabolism, despite its lower affinity for oxygen than cytochrome oxidase.