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Directed growth and fusion of membrane-wall microdomains requires CASP-mediated inhibition and displacement of secretory foci

Author

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  • Inês Catarina Ramos Barbosa

    (University of Lausanne)

  • Damien De Bellis

    (University of Lausanne)

  • Isabelle Flückiger

    (University of Lausanne)

  • Etienne Bellani

    (University of Lausanne)

  • Mathieu Grangé-Guerment

    (University of Lausanne)

  • Kian Hématy

    (University of Lausanne
    Université Paris-Saclay)

  • Niko Geldner

    (University of Lausanne)

Abstract

Casparian strips (CS) are aligned bands of lignin-impregnated cell walls, building an extracellular diffusion barrier in roots. Their structure profoundly differs from tight junctions (TJ), analogous structures in animals. Nonetheless, CS membrane domain (CSD) proteins 1-5 (CASP1-5) are homologues of occludins, TJ components. CASP-marked membranes display cell wall (matrix) adhesion and membrane protein exclusion. A full CASP knock-out now reveals CASPs are not needed for localized lignification, since correctly positioned lignin microdomains still form in the mutant. Ultra-structurally, however, these microdomains are disorganized, showing excessive cell wall growth, lack of exclusion zone and matrix adhesion, and impaired exocyst dynamics. Proximity-labelling identifies a Rab-GTPase subfamily, known exocyst activators, as potential CASP-interactors and demonstrate their localization and function at the CSD. We propose that CASP microdomains displace initial secretory foci by excluding vesicle tethering factors, thereby ensuring rapid fusion of microdomains into a membrane-cell wall band that seals the extracellular space.

Suggested Citation

  • Inês Catarina Ramos Barbosa & Damien De Bellis & Isabelle Flückiger & Etienne Bellani & Mathieu Grangé-Guerment & Kian Hématy & Niko Geldner, 2023. "Directed growth and fusion of membrane-wall microdomains requires CASP-mediated inhibition and displacement of secretory foci," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37265-7
    DOI: 10.1038/s41467-023-37265-7
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    References listed on IDEAS

    as
    1. Damien De Bellis & Lothar Kalmbach & Peter Marhavy & Jean Daraspe & Niko Geldner & Marie Barberon, 2022. "Extracellular vesiculo-tubular structures associated with suberin deposition in plant cell walls," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Daniele Roppolo & Bert De Rybel & Valérie Dénervaud Tendon & Alexandre Pfister & Julien Alassimone & Joop E. M. Vermeer & Misako Yamazaki & York-Dieter Stierhof & Tom Beeckman & Niko Geldner, 2011. "A novel protein family mediates Casparian strip formation in the endodermis," Nature, Nature, vol. 473(7347), pages 380-383, May.
    3. Guilhem Reyt & Priya Ramakrishna & Isai Salas-González & Satoshi Fujita & Ashley Love & David Tiemessen & Catherine Lapierre & Kris Morreel & Monica Calvo-Polanco & Paulina Flis & Niko Geldner & Yann , 2021. "Two chemically distinct root lignin barriers control solute and water balance," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    4. Syed Mukhtar Ahmed & Hisayo Nishida-Fukuda & Yuchong Li & W. Hayes McDonald & Claudiu C. Gradinaru & Ian G. Macara, 2018. "Exocyst dynamics during vesicle tethering and fusion," Nature Communications, Nature, vol. 9(1), pages 1-17, December.
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