Activity and functional interaction of alternative oxidase and uncoupling protein in mitochondria from tomato fruit

Abstract

Cyanide-resistant alternative oxidase (AOX) is not limited to plant mitochondria and is widespread among several types of protists. The uncoupling protein (UCP) is much more widespread than previously believed, not only in tissues of higher animals but also in plants and in an amoeboid protozoan. The redox energy-dissipating pathway (AOX) and the proton electrochemical gradient energy-dissipating pathway (UCP) lead to the same final effect, i.e., a decrease in ATP synthesis and an increase in heat production. Studies with green tomato fruit mitochondria show that both proteins are present simultaneously in the membrane. This raises the question of a specific physiological role for each energy-dissipating system and of a possible functional connection between them (shared regulation). Linoleic acid, an abundant free fatty acid in plants which activates UCP, strongly inhibits cyanide-resistant respiration mediated by AOX. Moreover, studies of the evolution of AOX and UCP protein expression and of their activities during post-harvest ripening of tomato fruit show that AOX and plant UCP work sequentially: AOX activity decreases in early post-growing stages and UCP activity is decreased in late ripening stages. Electron partitioning between the alternative oxidase and the cytochrome pathway as well as H + gradient partitioning between ATP synthase and UCP can be evaluated by the ADP/O method. This method facilitates description of the kinetics of energy-dissipating pathways and of ATP synthase when state 3 respiration is decreased by limitation of oxidizable substrate.

Differential Expression of Alternative Oxidase Genes in Maize Mitochondrial Mutants

“…Recent expression studies of two energy-dissipating pathways in plant mitochondria, represented by AOX and UCP, gave conflicting results regarding whether they function together or sequentially (Sluse and Jarmuszkiewicz, 2000;Considine et al, 2001). We observed only low levels of ucp transcripts in the NCS mutants, with some increase in NCS4, suggesting that AOX is used preferentially in maize when the ETC is blocked constitutively.…”

“…UCPs facilitate fatty acid-dependent proton reuptake through the inner mitochondrial membrane, causing dissipation of the electrochemical gradient as heat (Garlid et al, 1996). Like mammalian UCPs, plant UCP homologs can be regulated by cold, and like AOX, they are postulated to decrease ROS production (Laloi et al, 1997;Kowaltowski et al, 1998;Sluse and Jarmuszkiewicz, 2000). Figure 9B shows the expression of two maize ucp genes that were identified by their amino acid similarities to cold-inducible potato UCP (StUCP; Nantes et al, 1999) and cold-insensitive wheat UCP1a (TaUCP; Murayama and Handa, 2000).…”

The role of alternative oxidase in tomato fruit ripening and its regulatory interaction with ethylene

“…To date, limited information exists on the contribution of the AOX pathway to fruit ripening. Some reports suggested that the expression of AOX and the CN-insensitive respiration of isolated mitochondria decreased during post-harvest ripening of tomato (Almeida et al ., 1999; Costa et al ., 1999; Sluse and Jarmuszkiewicz, 2000). Nevertheless, Holtzapffel et al .…”

Changes in Mitochondrial Electron Partitioning in Response to Herbicides Inhibiting Branched-Chain Amino Acid Biosynthesis in Soybean

“…The physiological role of this pathway remains to be clarified except in the specialized case of promoting thermogenesis during flowering in aroid spadices (Meeuse, 1975;Moore and Siedow, 1991). However, several hints on the function of AOX have been achieved during the last decade and tend to indicate that AOX might have a function related to stress situations; for example, cold (Purvis and Shewfelt, 1993;Gonzàlez-Meler et al, 1999), oxygen radicals (Purvis, 1997;Yip and Vanlerberghe, 2001), phosphate starvation (Parsons et al, 1999;Gonzàlez-Meler et al, 2001), pathogen infection (Simons et al, 1999), and also in fruit ripening (Sluse and Jarmuszkiewicz, 2000;Considine et al, 2001) and hypersensitive response after pathogen infection (Xie and Chen, 2000;Ordog et al, 2002). Recently, Vanlerberghe et al (2002) and Robson and Vanlerberghe (2002), using different death-inducing compounds, suggested a possible role of AOX in programmed cell death, either preventing or attenuating whole plant death.…”