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Cell cycle-dependent changes in Golgi stacks, vacuoles, clathrin-coated vesicles and multivesicular bodies in meristematic cells of Arabidopsis thaliana: A quantitative and spatial analysis

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Abstract

Cytokinesis in plants involves both the formation of a new wall and the partitioning of organelles between the daughter cells. To characterize the cellular changes that accompany the latter process, we have quantitatively analyzed the cell cycle-dependent changes in cell architecture of shoot apical meristem cells of Arabidopsis thaliana. For this analysis, the cells were preserved by high-pressure freezing and freeze-substitution techniques, and their Golgi stacks, multivesicular bodies, vacuoles and clathrin-coated vesicles (CCVs) characterized by means of serial thin section reconstructions, stereology and electron tomography techniques. Interphase cells possess ∼35 Golgi stacks, and this number doubles during G2 immediately prior to mitosis. At the onset of cytokinesis, the stacks concentrate around the periphery of the growing cell plate, but do not orient towards the cell plate. Interphase cells contain ∼18 multivesicular bodies, most of which are located close to a Golgi stack. During late cytokinesis, the appearance of a second group of cell plate-associated multivesicular bodies coincides with the onset of CCV formation at the cell plate. During this period a 4× increase in CCVs is paralleled by a doubling in number and a 4× increase in multivesicular bodies volume. The vacuole system also undergoes major changes in organization, size, and volume, with the most notable change seen during early telophase cytokinesis. In particular, the vacuoles form sausage-like tubular compartments with a 50% reduced surface area and an 80% reduced volume compared to prometaphase cells. We postulate that this transient reduction in vacuole volume during early telophase provides a means for increasing the volume of the cytosol to accommodate the forming phragmoplast microtubule array and associated cell plate-forming structures.

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Abbreviations

CCV:

Clathrin-coated vesicle

dn:

Mean nuclear diameter

Dn:

Corrected mean nuclear diameter

EM:

Electron microscopy

ER:

Endoplasmic reticulum

MVB:

Multivesicular body

Na:

Plane numerical density

Nv:

Numerical density

Sv:

Surface density

TGN:

Trans-Golgi network

Vv:

Volume density

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Acknowledgements

We thank Mr. Ricardo Mantilla (CIRES, University of Colorado, Boulder, CO, USA) and Prof. Jaime Renau-Piqueras (Centro de Ïnvestigación Hospital “La Fe”, Valencia, Spain) for their mathematical advice, and Mrs. Erin White (MCDB, University of Colorado, Boulder, CO, USA) for her valuable help. Many thanks are also due to David Mastronarde and the rest of members of the Boulder Laboratory for 3-Dimensional Electron Microscopy of Cells (MCDB, University of Colorado, Boulder, CO, USA, Grant RR00592). This work was supported by National Institute of Health Grant GM 61306 to L.A.S.

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  1. José M. Seguí-Simarro

    Present address: Centro de Conservación y Mejora de la Agrodiversidad Valenciana (COMAV), Universidad Politécnica de Valencia, Camino de Vera, s/n, edificio 9B, 46022, Valencia, Spain

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  1. Department of Molecular, Cellular and Developmental Biology, University of Colorado, UCB 347, Boulder, CO, 80309-0347, USA

    José M. Seguí-Simarro & L. Andrew Staehelin

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  1. José M. Seguí-Simarro
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Correspondence to José M. Seguí-Simarro.

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Seguí-Simarro, J.M., Staehelin, L.A. Cell cycle-dependent changes in Golgi stacks, vacuoles, clathrin-coated vesicles and multivesicular bodies in meristematic cells of Arabidopsis thaliana: A quantitative and spatial analysis. Planta 223, 223–236 (2006). https://doi.org/10.1007/s00425-005-0082-2

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