Journal Article

A receptor-like kinase mutant with absent endodermal diffusion barrier displays selective nutrient homeostasis defects

Pfister, Alexandre, Barberon, Marie, Geldner, Niko, Kalmbach, Lothar, Li, Guowei, Vermeer, Joop EM, Maurel, Christophe, Alassimone, Julien, Lee, Yuree, Roppolo, Daniele, Yamazaki, Misako, Salt, David E, Takano, Junpei, Kamiya, Takehiro

2014

Overview

The endodermis represents the main barrier to extracellular diffusion in plant roots, and it is central to current models of plant nutrient uptake. Despite this, little is known about the genes setting up this endodermal barrier. In this study, we report the identification and characterization of a strong barrier mutant, schengen3 (sgn3). We observe a surprising ability of the mutant to maintain nutrient homeostasis, but demonstrate a major defect in maintaining sufficient levels of the macronutrient potassium. We show that SGN3/GASSHO1 is a receptor-like kinase that is necessary for localizing CASPARIAN STRIP DOMAIN PROTEINS (CASPs)—major players of endodermal differentiation—into an uninterrupted, ring-like domain. SGN3 appears to localize into a broader band, embedding growing CASP microdomains. The discovery of SGN3 strongly advances our ability to interrogate mechanisms of plant nutrient homeostasis and provides a novel actor for localized microdomain formation at the endodermal plasma membrane. Plant roots forage in the soil for minerals and water, but they must also provide a barrier that stops these nutrients leaking back out of the plant and stops microbes invading and causing disease. The endodermis—an inner layer of cells that surrounds the veins that run along the middle of a root—acts as such a barrier in young roots. Polymers that repel water are deposited between the cells in the roots of almost all vascular plants—which include ferns, conifers, and flowering plants—to form a band around the endodermis called the ‘Casparian strip’. This strip seals off the young roots and stops water moving through the gaps between plant cells, but still allows minerals, nutrients, and water to be transported through the root cells and into the plant. However, the importance of this structure has yet to be tested due to the lack of mutant plants without a Casparian strip. Pfister et al. now report that deleting the gene that encodes a protein called SCHENGEN3 in the model plant Arabidopsis thaliana causes the Casparian strip to be interrupted by irregularly sized holes. This protein is normally found at high levels in the root endodermis, where it is embedded into the cell membranes. Pfister et al. also showed that without the SCHENGEN3 protein, other proteins called CASPs—that normally mark out a stripe around the root cells where the Casparian strip will form—only accumulated in discontinuous patches. Further experiments revealed that deleting the gene for SCHENGEN3 does not cause general problems in delivering the CASP proteins to the cell membrane; instead, it specifically stops the CASP proteins from forming a single, uninterrupted stripe. Unexpectedly, disrupting the Casparian strip did not appear to hinder many of the functions of a root. The mutant plants could still take up water and nutrients, and the leaves of mutant plants had normal levels of many essential minerals—with the exception of potassium. The level of this mineral was much lower in mutant plants without the SCHENGEN3 protein. Pfister et al. suggest that in plants that lack an intact Casparian strip, potassium is continuously leaked from the root into the soil. These findings reveal that in Arabidopsis, at least, the Casparian strip might not be as important as once thought for helping the plant to take up and accumulate water and nutrients. Further work is now needed to uncover the as yet unknown backup systems that might be able to compensate for the loss of this structure.

• Publisher: eLife Sciences Publications Ltd,eLife Sciences Publication,eLife Sciences Publications, Ltd
• Subject: Arabidopsis - genetics / Arabidopsis - metabolism / Arabidopsis Proteins - genetics / Arabidopsis Proteins - metabolism / Biological Transport - genetics / Cell Biology / Cell Differentiation - genetics / COP9 Signalosome Complex / Defects / Deoxyribonucleic acid / Diffusion / DNA / Embedding / Gene Expression Profiling / Gene Expression Regulation, Plant / Genotype & phenotype / Homeostasis / Homeostasis - genetics / Kinases / Life Sciences / Lignin / Lipids - biosynthesis / Localization / Microscopy, Confocal / Mutation / Nuclear Proteins - genetics / Nuclear Proteins - metabolism / Nutrient uptake / Oligonucleotide Array Sequence Analysis / Plant Biology / plant nutrition / Plant Roots - cytology / Plant Roots - genetics / Plant Roots - metabolism / Plants, Genetically Modified / Plasma / polarity / Potassium - metabolism / Protein Kinases - genetics / Protein Kinases - metabolism / Proteins / Reverse Transcriptase Polymerase Chain Reaction / root biology / Vegetal Biology / Water - metabolism