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Tip-localized actin polymerization and remodeling, reflected by the localization of ADF, profilin and villin, are fundamental for gravity-sensing and polar growth in characean rhizoids

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Abstract

Polar organization and gravity-oriented, polarized growth of characean rhizoids are dependent on the actin cytoskeleton. In this report, we demonstrate that the prominent center of the Spitzenkörper serves as the apical actin polymerization site in the extending tip. After cytochalasin D-induced disruption of the actin cytoskeleton, the regeneration of actin microfilaments (MFs) starts with the reappearance of a flat, brightly fluorescing actin array in the outermost tip. The actin array rounds up, produces actin MFs that radiate in all directions and is then relocated into its original central position in the center of the Spitzenkörper. The emerging actin MFs rearrange and cross-link to form the delicate, subapical meshwork, which then controls the statolith positioning, re-establishes the tip-high calcium gradient and mediates the reorganization of the Spitzenkörper with its central ER aggregate and the accumulation of secretory vesicles. Tip growth and gravitropic sensing, which includes control of statolith positioning and gravity-induced sedimentation, are not resumed until the original polar actin organization is completely restored. Immunolocalization of the actin-binding proteins, actin-depolymerizing factor (ADF) and profilin, which both accumulate in the center of the Spitzenkörper, indicates high actin turnover and gives additional support for the actin-polymerizing function of this central, apical area. Association of villin immunofluorescence with two populations of thick undulating actin cables with uniform polarity underlying rotational cytoplasmic streaming in the basal region suggests that villin is the major actin-bundling protein in rhizoids. Our results provide evidence that the precise coordination of apical actin polymerization and dynamic remodeling of actin MFs by actin-binding proteins play a fundamental role in cell polarization, gravity sensing and gravity-oriented polarized growth of characean rhizoids.

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Fig. 1a–c
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Abbreviations

ADF :

Actin-depolymerizing factor

CD :

Cytochalasin D

MF :

Microfilament

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Acknowledgements

We thank Andreas Sievers and Brigitte Buchen for stimulating discussions and critical reading of the manuscript, Diedrik Menzel for giving us the opportunity to work with the confocal microscope, Simone Masberg for excellent technical assistance (all University of Bonn, Germany). We are grateful to Chris Staiger (Purdue University, USA) for kindly providing antibodies against ADFs, profilins and fimbrin, Luis Vidali (University of Massachussetts, USA) for the generous gift of the villin antibody and Frantisek Baluška (Universität Bonn, Germany) for sharing anti-HDEL. This work was financially supported by Deutsches Zentrum für Luft- und Raumfahrt (DLR) on behalf of the Bundesministerium für Bildung und Forschung (50WB9998). C.L. receives financial support from a Cusanus fellowship.

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Authors and Affiliations

  1. Institut für Molekulare Physiologie und Biotechnologie der Pflanzen, Universität Bonn, Venusbergweg 22, 53115, Bonn, Germany

    Markus Braun, Jens Hauslage & Christoph Limbach

  2. Institute of Biochemistry and Molecular Biology, Department of Cytobiochemistry, University of Wroclaw, ul. Przbyszewskiego 63–77, 51-148, Wroclaw, Poland

    Aleksander Czogalla

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  1. Markus Braun
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Correspondence to Markus Braun.

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Braun, M., Hauslage, J., Czogalla, A. et al. Tip-localized actin polymerization and remodeling, reflected by the localization of ADF, profilin and villin, are fundamental for gravity-sensing and polar growth in characean rhizoids. Planta 219, 379–388 (2004). https://doi.org/10.1007/s00425-004-1235-4

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