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The mitochondrial compartment (Logan, 2006)

This review article focuses on compartmentalization and the requirements from an energy-generating perspective. It is clear that many conformations exist in different cell types and within development, and it is the nucleus that seems to orchestrate the different roles the mitochondrion can play.

The role of the mitochondrion in the synthesis of ATP formed by oxidative phosphorylation is well established (Saraste, 1999) and, in addition, mitochondria are involved in numerous other metabolic processes including the biosynthesis of amino acids, vitamin cofactors, fatty acids, and iron-sulphur clusters (Mackenzie and McIntosh, 1999; Bowsher and Tobin, 2001). Apart from the role of the mitochondrion in ATP synthesis and various biosynthetic pathways the mitochondrion is one of three cell compartments involved in photorespiration (Douce and Neuburger, 1999), is implicated in cell signalling (Vandecasteele et al., 2001; Logan and Knight, 2003), and has been shown recently to be involved in programmed cell death (Jones, 2000; Youle and Karbowski, 2005).

The energy-transducing membrane is central to the chemiosmotic theory that explains the basic mechanism of biological energy production, whereby ATP production is coupled to the controlled dissipation of a proton electrochemical gradient (proton motive force). The membrane allows compartmentalization of protons, via their vectorial transport across the membrane, by the action of a primary proton pump(s). In mitochondria the primary proton pumps comprise complexes I, III, and IV. These primary pumps generate a high gradient of protons that forces a secondary pump (the ATP synthase complex) to reverse, energized by the flow of protons ‘downhill’, thereby synthesizing ATP from ADP and Pi. Any proton leak across the membrane would cause a short-circuit, destroy the compartmentalization of protons and uncouple the proton motive force from the ATP synthase. The energy-transducing membrane must, therefore, be essentially closed and have a high resistance to proton flux.

What is clear from the above discussion is that at least six discrete mitochondrial compartments can be recognized on a structural basis: outer membrane, intermembrane space, inner boundary membrane, cristal membrane, intercristal space, and matrix.

Mitochondrial inheritance is maternal in the majority of angiosperms (Mogensen, 1988) and therefore represents a form of extreme compartmentalization whereby paternal mtDNA is excluded or removed from the zygote. In contrast to the mechanism in mammals, wherein sperm mitochondria are ubiquitinated during spermatogenesis leading to their specific degradation in the zygote (Sutovsky et al., 1996, 1999a, 2003; Thompson et al., 2003), maternal inheritance in angiosperms appears to occur primarily as a result of the exclusion of paternal mitochondrial genomes from the male reproductive cells before fertilization (Nagata et al., 1999a, b; Sodmergen et al., 2002), although a mechanism similar to that active in mammals may also operate in angiosperms (Liu et al., 2004).

However, it is clear that many physically discrete mitochondria within a plant cell contain less than a full genome (Lonsdale et al., 1988). To account for the observed complexity of the mitochondrial genomes of higher plants, Lonsdale et al. (1988) proposed that the mitochondria form a ‘dynamic syncytium’ and that the mitochondrial population within a cell is panmictic (via organelle fusion and fission) and, as a result, in a state of recombinational equilibrium. Inter-mitochondrial recombination has been demonstrated in tobacco cybrids (Belliard et al., 1979) and complementation between fused mitochondria is now believed to be a common mechanism to counter the accumulation of mtDNA mutations in mammalian mitochondria (Nakada et al., 2001; Ono et al., 2001).

Without compartmentalization, mitochondria would not be able to convert the potential energy stored in respiratory substrates into ATP. However, being a semi-autonomous organelle, containing its own DNA, is not compatible with the mitochondrion’s role as provider of energy. This conflict of interests, between energy provider (hence ROS generator) and genetic vault, has been overcome in plants by a series of features including: (i) compartmentalization of the chondriome into a series of physically discrete mitochondria (a ‘discontinuous whole’), (ii) the organization of the mitochondrial genome in a multipartite highly replicated structure and its distribution amongst the discrete mitochondria in (frequently) sub-genomic proportions, (iii) inter-mitochondrial complementation to mitigate against the accumulation of mtDNA lesions in any given physically discrete organelle, either by panmictic fusion of discrete mitochondria in non-dividing cells or during the MMF prior to cell division, and (iv) anisogamy in most angiosperms to ensure the inheritance of undamaged mitochondria and mtDNA. Future research using the latest advances in bioimaging and functional genomics will help to answer questions about the division of labour amongst the physically discrete members of the higher plant chondriome of somatic cells. For example, whether or not individual mitochondria within any given cell are specialized for bioenergetics, biosynthesis, ROS monitoring/ signalling, or PCD induction.

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