Alternative oxidase respiration maintains both mitochondrial and chloroplast function during drought

The mitochondrial electron transport chain (ETC) terminates at cytochrome (cyt) oxidase or alternative oxidase (AOX). In Nicotiana tabacum leaves, mitochondrial respiration in the light (R-L) declined with increasing drought severity but then increased under extreme drought, despite a steep decline in maximal cyt oxidase activity. This increased R-L was absent in AOX knockdown lines, while AOX overexpression lines showed enhanced R-L relative to the wild-type (WT). Cyt oxidase activity under extreme drought was higher in overexpressors and lower in knockdowns, compared with the WT, providing evidence that AOX acted to maintain cyt pathway function. The rate of R-L was a strong determinant of the reduction state of the photosynthetic ETC during drought. As such, the maximal quantum yield of photosystem II was compromised in knockdowns, compared with the WT, during extreme drought. By contrast, overexpressors maintained their instantaneous leaf water-use efficiency equally as high during extreme drought as when they were well watered. In both mitochondria and chloroplasts, protein carbonyl accumulation during extreme drought was strongly increased in knockdowns, and decreased in overexpressors, relative to WT. Hence the ability of AOX to maintain critical mitochondrial and chloroplast functions during extreme drought is likely due, at least in part, to its ability to reduce oxidative damage.