Plant Mitochondria

Abstract

Plant mitochondria, like the mitochondria of most other eukaryotes, use an electron transport chain (ETC) to translocate protons and generate adenosine triphosphate (ATP). The generation of ATP through mitochondrial respiration also produces reactive oxygen species (ROS). In excess, ROS can damage the cell, but they are also an important signal produced in response to varied stresses. In addition to the classical electron transport chain, plant mitochondria possess an alternative ETC that can limit proton translocation (ATP synthesis) and modulate mitochondrial ROS production. Because mitochondria depend on proteins encoded by both mitochondrial and nuclear genomes, a sophisticated two‐way communication between the two organelles exists to ensure correct mitochondrial biogenesis and function. A balance of fusion and fission controls the morphology and number of plant mitochondria and is important for functionality and inheritance of their multipartite genome – an important determinant of male fertility.

Key Concepts:

  • Plant mitochondria are frequently small (1–2 μm long) but are highly pleomorphic and undergo frequent fusion and fission events.

  • Plant mitochondria have a smooth outer membrane and a highly convoluted inner membrane housing an electron transport chain (ETC) that drives adenosine triphosphate (ATP) synthesis.

  • In mitochondria, the production of reactive oxygen species (ROS) is inextricably linked to the production of ATP through oxidative phosphorylation.

  • ROS can damage macromolecules, but are important stress signalling molecules.

  • The alternative oxidase is a major component of the alternative ETC and can modulate ROS and ATP production.

  • There are approximately 2000 proteins in plant mitochondria mainly encoded by the nuclear genome with a smaller contribution from the mitochondrial genome.

  • Mitochondria participate in the biosynthesis of a range of coenzymes and vitamins.

  • Photorespiration, necessitated by the oxygenase activity of the carbon dioxide fixing enzyme ribulose‐1,5‐bisphosphate carboxylase/oxygenase (RuBisCO), involves interactions between chloroplasts, mitochondria and peroxisomes.

  • The nucleus controls mitochondrial gene expression (anterograde control), yet mitochondria can also influence nuclear gene expression (retrograde control).

  • Disrupted plant mitochondrial function often causes cytoplasmic male sterility (CMS) by perturbing pollen development.

Keywords: alternative oxidase; anterograde and retrograde signalling; cytoplasmic male sterility; electron transport chain; mitochondrial fusion; mitochondrial genome; plant mitochondria; reactive oxygen species

Figure 1.

Cycle of mitochondrial fusion and fission before plant cells reinitiate cell division. Based on study of Sheahan et al. using cultured Nicotiana tabacum mesophyll protoplasts expressing GFP targeted to mitochondria by the cytochrome oxidase IV signal peptide from yeast. (a) Mitochondria are initially, small oval‐shaped organelles. (b) Early in protoplast culture, before DNA synthesis, mitochondria undergo a phase of massive elongation, caused by mitochondrial fusion. (c) Following the fusion phase, mitochondria undergo fission, generating large numbers of small mitochondria. (d) Large numbers of uniformly dispersed mitochondria enhance unbiased inheritance of the organelle at cell division. Bar, 10 μm. Reproduced from Sheahan et al. , with permission of Blackwell Publishing.

Figure 2.

Demonstration of mitochondrial fusion in plant protoplasts. Based on study of Sheahan et al. showing fusion of cultured tobacco mesophyll protoplasts containing either MitoTracker‐labelled mitochondria or mitochondrially targeted GFP. (a) Schematic diagram indicating the process of mitochondrial fusion and the resulting colour change from overlay of red and green mitochondrial labels. (b) A protoplast with MitoTracker‐labelled mitochondria. (c) A protoplast expressing mitochondrially targeted GFP. (d) A fused protoplast after 24 h culture. Many mitochondria present are yellow because of colocalised labels, indicating mitochondrial fusion has occurred. Bar, 10 μm. Reproduced from Sheahan et al. , with permission of Blackwell Publishing.

Figure 3.

Organisation of mitochondrial membranes and the electron transport chain. (a) False‐coloured transmission electron micrograph of a mitochondrion from Vicia faba and corresponding schematic diagram showing the organisation of mitochondrial membranes and division of the mitochondrion into six distinct compartments. (b) The mitochondrial ETC of a typical plant. The five complexes (complexes I–IV and ATP synthase) common to the standard ETC are shown in gold. Plant‐specific complexes (AOX and NAD(P)H oxidoreductases) are shown in green, whereas mobile electron carriers, ubiquinone and cytochrome c, are shown in red. An uncoupling ND, NAD(P)H oxidoreductase; UQ, ubiquinone; AOX, alternate terminal oxidase; Cyt C, cytochrome c; PUMP, plant uncoupling mitochondrial protein. Protons are pumped from the matrix into the intermembrane and intercristal spaces. Bar, 0.1 μm. Electron micrograph, X–D Wang; drawings, MB Sheahan.

Figure 4.

Intracellular communications within the cell. The nucleus controls mitochondrial (as well as plastid gene expression) through anterograde signalling controls. Organelles communicate with the nucleus (retrograde signalling) to regulate nuclear gene expression. Organelles within a cell also communicate with one another through pathways of organelle crosstalk.

Figure 5.

Flower morphology of Nicotiana tabacum (+) Nicotiana suaveolens cybrids. Nucleus is N. tabacum and with recombined mtDNA from N. tabacum and N. suaveolens (a, b) Flower morphology. (a) Nicotiana tabacum flower with and without petals showing carpel and stamens. (b) Cybrid flower with and without petals showing carpel and carpelloid‐stamens and split corolla. (c, d) Scanning electron micrographs of dissected buds. (c) Nicotiana tabacum stamens surround carpel. (d) Cybrid bud showing whorl of carpelloid‐stamens surrounding carpel. Bar, 1 cm (a, b) and 1 mm (c, d). Photographs, J.T. Fitter and M.R. Thomas from authors’ laboratory. Reprinted from Fitter et al. , © 2005, with permission by Elsevier.

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Rose, Ray J, and Sheahan, Michael B(May 2012) Plant Mitochondria. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001680.pub2]