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CELL BIOLOGY AND SIGNAL TRANSDUCTION

The Mitochondrial Cycle of Arabidopsis Shoot Apical Meristem and Leaf Primordium Meristematic Cells Is Defined by a Perinuclear Tentaculate/Cage-Like Mitochondrion^1,[W],[OA]

Instituto para la Conservación y Mejora de la Agrodiversidad Valenciana, Universidad Politécnica de Valencia, Ciudad Politécnica de la Innovación, 46022 Valencia, Spain (J.M.S.-S.); Centro de Investigaciones Biologicas, Consejo Superior de Investigaciones Científicas, 28040 Madrid, Spain (M.J.C.); and Department of Molecular, Cellular, and Developmental Biology, University of Colorado, Boulder, Colorado 80309–0347 (L.A.S.)

Plant cells exhibit a high rate of mitochondrial DNA (mtDNA) recombination. This implies that before cytokinesis, the different mitochondrial compartments must fuse to allow for mtDNA intermixing. When and how the conditions for mtDNA intermixing are established are largely unknown. We have investigated the cell cycle-dependent changes in mitochondrial architecture in different Arabidopsis (Arabidopsis thaliana) cell types using confocal microscopy, conventional, and three-dimensional electron microscopy techniques. Whereas mitochondria of cells from most plant organs are always small and dispersed, shoot apical and leaf primordial meristematic cells contain small, discrete mitochondria in the cell periphery and one large, mitochondrial mass in the perinuclear region. Serial thin-section reconstructions of high-pressure-frozen shoot apical meristem cells demonstrate that during G1 through S phase, the large, central mitochondrion has a tentaculate morphology and wraps around one nuclear pole. In G2, both types of mitochondria double their volume, and the large mitochondrion extends around the nucleus to establish a second sheet-like domain at the opposite nuclear pole. During mitosis, approximately 60% of the smaller mitochondria fuse with the large mitochondrion, whose volume increases to 80% of the total mitochondrial volume, and reorganizes into a cage-like structure encompassing first the mitotic spindle and then the entire cytokinetic apparatus. During cytokinesis, the cage-like mitochondrion divides into two independent tentacular mitochondria from which new, small mitochondria arise by fission. These cell cycle-dependent changes in mitochondrial architecture explain how these meristematic cells can achieve a high rate of mtDNA recombination and ensure the even partitioning of mitochondria between daughter cells.

² Present address: PROJECH, Parque Científico de Madrid, C/Santiago Grisolía 2, Parque Tecnológico de Madrid, 28760 Tres Cantos, Madrid, Spain.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: José M. Seguí-Simarro (seguisim{at}btc.upv.es).

^[W] The online version of this article contains Web-only data.

^[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.126953

^* Corresponding author; e-mail seguisim{at}btc.upv.es.

Received August 19, 2008; accepted September 13, 2008; published September 17, 2008.

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Peter V. Minorsky
Plant Physiol. 2008 148: 1185-1186. [Full Text]