Abstract
Polarized epithelia are fundamental to multicellular life. In animal epithelia, conserved junctional complexes establish membrane diffusion barriers, cellular adherence and sealing of the extracellular space1. Plant cellular barriers are of independent evolutionary origin. The root endodermis strongly resembles a polarized epithelium and functions in nutrient uptake and stress resistance2. Its defining features are the Casparian strips, belts of specialized cell wall material that generate an extracellular diffusion barrier2. The mechanisms localizing Casparian strips are unknown. Here we identify and characterize a family of transmembrane proteins of previously unknown function. These ‘CASPs’ (Casparian strip membrane domain proteins) specifically mark a membrane domain that predicts the formation of Casparian strips. CASP1 displays numerous features required for a constituent of a plant junctional complex: it forms complexes with other CASPs; it becomes immobile upon localization; and it sediments like a large polymer. CASP double mutants display disorganized Casparian strips, demonstrating a role for CASPs in structuring and localizing this cell wall modification. To our knowledge, CASPs are the first molecular factors that are shown to establish a plasma membrane and extracellular diffusion barrier in plants, and represent a novel way of epithelial barrier formation in eukaryotes.
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Sequences have been deposited in GenBank under accession code HQ699533-50.
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Acknowledgements
We thank the Central Imaging Facility (CIF) and the Protein Analysis Facility (PAF) of the University of Lausanne for technical support, G. Jürgens, W. Michalke, J. Chory for antibodies, T. W. J. Gadella for mTurquoise and J. Takano for mutant BOR1 clone. We thank J. Chory, E. M. N. Dohmann, Y. Lee and G. Jürgens for comments and critical reading of the manuscript. This work was supported by grants of the Swiss National Science Foundation and the European Research Council (ERC) to N.G., the Belgian Interuniversity Attraction Poles program (IUAP VI/33) and the Special Research Fund of Ghent University to B.D.R. and T.B., the Roche Research Foundation to D.R. and a Marie-Curie IEF grant to J.E.M.V.
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N.G., D.R., B.D.R. and T.B. conceived and designed experiments. D.R., B.D.R., V.D.T., A.P., J.A., J.E.M.V., M.Y., Y.-D.S. and N.G. performed the experiments. D.R., B.D.R., V.D.T., A.P., J.A., J.E.M.V., Y.-D.S. and N.G. analysed the data. N.G. and D.R. wrote the manuscript.
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Supplementary information
Supplementary Information
This file contains Supplementary Figures 1-12 with legends and legends for Supplementary Movies 1-3. (PDF 1083 kb)
Supplementary Movie 1
This movie shows ring-like CASP1-GFP localization tightly coordinated between cells - see Supplementary Information file for full legend. (AVI 21318 kb)
Supplementary Movie 2
This movie shows non-localized CASP1-GFP rapidly accumulated in a central ring - see Supplementary Information file for full legend. (AVI 1649 kb)
Supplementary Movie 3
This movie shows CASP1-GFP band formation through fusion of individual patches - see Supplementary Information file for full legend. (AVI 1710 kb)
Supplementary Movie 4
This movie shows comparison of CS structure in wt and casp1-1;casp3-1 double mutants - see Supplementary Information file for full legend. (AVI 9663 kb)
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Roppolo, D., De Rybel, B., Tendon, V. et al. A novel protein family mediates Casparian strip formation in the endodermis. Nature 473, 380–383 (2011). https://doi.org/10.1038/nature10070
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DOI: https://doi.org/10.1038/nature10070
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