Abstract

The evolution of membrane-bound organelles among eukaryotes led to a highly compartmentalized metabolism. As a compartment of the central carbon metabolism, mitochondria must be connected to the cytosol by molecular gates that facilitate a myriad of cellular processes. Members of the mitochondrial carrier family function to mediate the transport of metabolites across the impermeable inner mitochondrial membrane and, thus, are potentially crucial for metabolic control and regulation. Here, we focus on members of this family that might impact intracellular central plant carbon metabolism. We summarize and review what is currently known about these transporters from in vitro transport assays and in planta physiological functions, whenever available. From the biochemical and molecular data, we hypothesize how these relevant transporters might play a role in the shuttling of organic acids in the various flux modes of the TCA cycle. Furthermore, we also review relevant mitochondrial carriers that may be vital in mitochondrial oxidative phosphorylation. Lastly, we survey novel experimental approaches that could possibly extend and/or complement the widely accepted proteoliposome reconstitution approach.

Highlights

  • An ancestral endosymbiotic α-proteobacteria fused with an ancestral eukaryotic cell to give rise to the mitochondria approximately 1.5 billion years ago [1]

  • The intracellular transport of mitochondrial metabolites plays an important role in cellular respiration via the processes of the tricarboxylic acid (TCA) cycle, oxidative phosphorylation, amino acids biosynthesis [3], fatty acids biosynthesis [4], photorespiration [5], and C4 photosynthesis [6]

  • Metabolic intermediates of these pathways pass through the double membrane of mitochondria that delineates four different sub-compartments: the outer mitochondrial membrane (OMM), the intermembrane space (IMS), the inner mitochondrial membrane (IMM), and the mitochondrial matrix (MM) [7]

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Summary

Introduction

An ancestral endosymbiotic α-proteobacteria fused with an ancestral eukaryotic cell to give rise to the mitochondria approximately 1.5 billion years ago [1]. In vitro biochemical data regarding mitochondrial organic acid transporters showed that these mitochondrial carriers are most likely responsible for shuttling of TCA cycle intermediates, i.e., between the cytosol and the mitochondria. There are three mitochondrial carriers most likely to be relevant to TCA cycle operation under different flux modes These are: (1) dicarboxylate carriers (DICs); (2) dicarboxylate/tricarboxylate carriers (DTC); and (3) succinate/fumarate carrier (SFC). ATP demand from cellular respiration is low and enzyme kinetic analysis suggests that this results in the operation of a non-cyclic flux mode [37] (Figure 2) In this model, pyruvate entry into the TCA is reduced since the pyruvate dehydrogenase complex is inactivated in the light by phosphorylation. It is likely that SFC is using another metabolite as a counter-substrate to facilitate fumarate transport, possibly OAA and 2-oxogulatrate, in congruence with yeast SFC transport assays [54]

Mitochondrial Carriers Relevant to Mitochondrial Oxidative Phosphorylation
Adenylate Transporters
Novel Approaches to Investigate MCFs
Findings
Perspectives
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