The uncoupling of respiration in plant mitochondria: keeping reactive oxygen and nitrogen species under control

Abstract

Plant mitochondrial respiration involves operation of various alternate pathways. These pathways participate, both directly and indirectly, in the maintenance of mitochondrial functions though they do not contribute to energy production being uncoupled from the generation of an electrochemical gradient across the mitochondrial membrane and thus from ATP production. Recent findings suggest that uncoupled respiration is involved in reactive oxygen species (ROS) and nitric oxide (NO) scavenging, regulation and homeostasis. Here we discuss specific roles and possible functions of the uncoupled mitochondrial respiration in ROS and NO metabolism. The mechanisms of expression and regulation of the NDA, NDB and NDC type non-coupled NADH and NADPH dehydrogenases, the alternative oxidase (AOX), and the uncoupling protein (UCP) are examined in relation to their involvement in the establishment of the stable far-from-equilibrium state of plant metabolism. The role of uncoupled respiration in controlling the levels of ROS and NO as well as inducing signaling events is considered. Secondary functions of uncoupled respiration include its role in protection from stress factors and roles in biosynthesis and catabolism. It is concluded that uncoupled mitochondrial respiration plays an important role in providing rapid adaptation of plants to changing environmental factors via regulation of ROS and NO.

γ-Aminobutyrate (GABA) Regulated Plant Defense: Mechanisms and Opportunities

“…A third route is also possible, involving the direct synthesis of Glu from 2-OG via the mitochondrial glutamate dehydrogenase (GDH) and then export via the uncoupling proteins AtUCP1,2 [ 90 , 91 ]. The UCP is known to decrease the electrochemical gradient across the mitochondrial inner membrane, and prevent the over-reduction of the mETC [ 92 ].…”

“…Cinnamyl alcohol dehydrogenase is involved in lignin biosynthesis and alkenyl reductase and can detoxify cytotoxic substrates such as aldehydes [ 155 ]. Further research is required to investigate the effects of exogenous GABA on alternative respiratory pathways involved in the scavenging, regulation and homeostasis of ROS and NO [ 92 , 191 ], the action of other phytohormones [ 23 , 156 , 187 , 192 , 193 , 194 , 195 , 196 , 197 ], and post-translational modifications and epigenetic regulation of gene expression [ 147 , 198 ] during stress.…”

Exploring the Contribution of Autophagy to the Excess-Sucrose Response in Arabidopsis thaliana

“…These included citrate synthase, and succinate dehydrogenase subunit 7, which significantly accumulated under sucrose excess in atg5-1 plants, and succinyl CoA ligase, which showed higher (but not significant) levels. Since uncoupler proteins can finetune the mitochondrial membrane potential, and consequently lead to a reduction in ROS production [ 61 , 62 , 63 , 64 ], these findings strongly suggest mitochondrial involvement in the root response to excess sucrose.…”

“…Mitochondrial uncouplers have been found essential for maintaining ROS homeostasis [ 61 , 62 , 63 , 64 ]. PUMP5, a mitochondrial uncoupler protein, accumulated massively in atg mutant plants under sucrose excess ( Table 2 ), suggesting its possible role in ROS homeostasis, with possible mitochondrial involvement in ROS production and response under excess sucrose.…”

Metabolism and Signaling of Plant Mitochondria in Adaptation to Environmental Stresses

“…AOX reduces electron flow through Complexes III and IV, decreasing the leakage of electrons to nitrite and, thus, suppressing NO accumulation. Excess NO can rapidly react with proteins and other free radicals, forming S -nitrosylated and tyrosine-nitrated proteins in addition to producing reactive nitrogen species (RNS) [ 60 , 61 ]. The relationship between AOX and NO scavenging was recently investigated using plants that were subjected to hypoxia or treated with flagellin (flg22) [ 60 , 62 ], as this elicitor also induces NO production [ 63 ].…”