CASP microdomain formation requires cross cell wall stabilization of domains and non-cell autonomous action of LOTR1

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Abstract

Efficient uptake of nutrients in both animal and plant cells requires tissue-spanning diffusion barriers separating inner tissues from the outer lumen/soil. However, we poorly understand how such contiguous three-dimensional superstructures are formed in plants. Here, we show that correct establishment of the plant Casparian Strip (CS) network relies on local neighbor communication. We show that positioning of Casparian Strip membrane domains (CSDs) is tightly coordinated between neighbors in wild-type and that restriction of domain formation involves the putative extracellular protease LOTR1. Impaired domain restriction in lotr1 leads to fully functional CSDs at ectopic positions, forming 'half strips'. LOTR1 action in the endodermis requires its expression in the stele. LOTR1 endodermal expression cannot complement, while cortex expression causes a dominant-negative phenotype. Our findings establish LOTR1 as a crucial player in CSD positioning acting in a directional, non-cell-autonomous manner to restrict and coordinate CS positioning.

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All data generated or analysed during this study are included in the manuscript and supporting files.

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Andreas Kolbeck

Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland

Competing interests
The authors declare that no competing interests exist.
Peter Marhavý

Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland

Competing interests
The authors declare that no competing interests exist.
Damien De Bellis

Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland

Competing interests
The authors declare that no competing interests exist.
Baohai Li

Department of Applied Biological Chemistry, University of Tokyo, Tokyo, Japan

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The authors declare that no competing interests exist.
Takehiro Kamiya

Department of Applied Biological Chemistry, University of Tokyo, Tokyo, Japan

Competing interests
The authors declare that no competing interests exist.
Toru Fujiwara

Department of Applied Biological Chemistry, University of Tokyo, Tokyo, Japan

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The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-5363-6040
Lothar Kalmbach

Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland

Competing interests
The authors declare that no competing interests exist.
Niko Geldner

Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland

For correspondence
niko.geldner@unil.ch

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-2300-9644

Funding

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (31003A_156261)

Niko Geldner

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (310030B_176399)

Niko Geldner

Federation of European Biochemical Societies

Peter Marhavý

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.