Alternative oxidase: a respiratory electron transport chain pathway essential for maintaining photosynthetic performance during drought stress

Abstract

Photosynthesis and respiration are the hubs of energy metabolism in plants. Drought strongly perturbs photosynthesis as a result of both diffusive limitations resulting from stomatal closure, and in some cases biochemical limitations that are associated with a reduced abundance of key photosynthetic components. The effects of drought on respiration, particularly respiration in the light (RL ), are less understood. The plant mitochondrial electron transport chain includes a non-energy conserving terminal oxidase called alternative oxidase (AOX). Several studies have shown that drought increases AOX transcript, protein and maximum capacity. Here we review recent studies comparing wild-type (WT) tobacco to transgenic lines with altered AOX protein amount. Specifically during drought, RL was compromised in AOX knockdown plants and enhanced in AOX overexpression plants, compared with WT. Significantly, these differences in RL were accompanied by dramatic differences in photosynthetic performance. Knockdown of AOX increased the susceptibility of photosynthesis to drought-induced biochemical limitations, while overexpression of AOX delayed the development of such biochemical limitations, compared with WT. Overall, the results indicate that AOX is essential to maintaining RL during drought, and that this non-energy conserving respiration maintains photosynthesis during drought by promoting energy balance in the chloroplast. This review also outlines several areas for future research, including the possibility that enhancement of non-energy conserving respiratory electron sinks may be a useful biotechnological approach to increase plant performance during stress.

Alternative oxidase and plant stress tolerance

“…Since both systems produce a large amount of energy, it is of utmost necessity to maintain coordination between the activities of chloroplasts and mitochondria in the light. 7 The expression of AOXs also is known to be induced by a wide range of biotic and abiotic stresses. 8,3 The induced expression of AOX genes under stress conditions is associated with stress-dependent reactive oxygen species (ROS) production.…”

“…27 It has been reported that, for several species of monocot and dicot leaves, drought stress can lead to an increase in the transcription of gene(s) encoding AOX, the amount of AOX protein, or the maximum capacity of the AOX pathway to consume electrons. 7 AOX controls respiration, photosynthesis and chlorophyll synthesis during drought to maintain an overall homeostasis and enhance plant lifespan. 7 AOX has also been reported to be responsible for development of cold resistance in winter wheat seedlings, whereas at temperatures below zero AOX activity slightly decreases.…”

“…7 AOX controls respiration, photosynthesis and chlorophyll synthesis during drought to maintain an overall homeostasis and enhance plant lifespan. 7 AOX has also been reported to be responsible for development of cold resistance in winter wheat seedlings, whereas at temperatures below zero AOX activity slightly decreases. 28 Phosphorous deficiency leads to shortage of adenylates and Pi, which are substrates for oxidative phosphorylation and hence AOX is induced to maintain electron flow.…”

Variation in relative water content, proline accumulation and stress gene expression in two cowpea landraces under drought

“…For example, mitochondrial alternative oxidase (AOX) isoforms can be induced by drought in plants, including cowpea, to limit mitochondrial ROS production (Vanlerberghe et al, 2016) (Costa et al, 2010) (Wang and Vanlerberghe, 2013). The plastid terminal oxidase PTOX, a chloroplast homologue of AOX, is induced in some plant species to limit excess electron transfer in the chloroplast during stress (Laureau et al, 2013) (Johnson and Stepien, 2016).…”

Analysis of Posttranslational Activation of Alternative Oxidase Isoforms

“…Studies in Arabidopsis and tobacco (Nicotiana tabacum) clearly revealed a role for AOX in the dissipation of excessive reducing power while maintaining photosynthesis under high-light stress (Florez-Sarasa et al, 2011Dahal et al, 2014Dahal et al, , 2015Vanlerberghe et al, 2016). In Arabidopsis, aox1a knockout plants cannot be complemented by the expression of other isogenes (Strodtkötter et al, 2009;Kühn et al, 2015).…”