Background image mask

LSSS 2016-2017


Life Sciences Seminar Series


Back to seminar list

Niko Geldner

Department of Plant Molecular Biology (DBMV), Université de Lausanne, Switzerland

The endodermis - the green version of a polarised epithelium

Talk abstract

The supracellular Casparian strip network of the endodermis is analogous to the tight/adherence junctions of an animal gut epithelium. Evolved independently from animals, the endodermis and its ring-like Casparian strip represents an intriguing study case of convergent evolution. The endodermis is a highly conserved feature of plant roots, thought to have evolved for balancing the need of a protective seal with that of continued uptake from and perception of the environment. How this intricate structure is built and how the plant manages to ensure a tight, tissue-spanning seal is unknown. In a forward genetic screen aimed at identifying factors involved in the formation of the endodermal diffusion barrier, we identified three mutants that displayed a similar, specific phenotype, consisting of a fragmented, but normally localised Casparian strip. While SCHENGEN 3 (SGN3) and SGN1 were found to encode an LRR receptor-like kinase and a receptor-like cytoplasmic kinase, respectively, SGN2 turned out to be identical to TPST, an enzyme responsible for sulfating peptide ligands. We therefore speculated that the SGN3-ligand might be a sulfated peptide, yet were able to exclude involvement of previously known ones. I will report on the identification of a stele expressed peptide that binds the SGN3 receptor ectodomain and complements the sgn2/tpst CS phenotype at nanomolar concentrations. Moreover, excess ligand leads to strong delocalisation of Casparian Strip domain proteins (CASPs), as well as to massive overlignification, specifically of the endodermis - effects that are entirely dependent on the presence of SGN3. I will propose a model as to the role of this SGN3-ligand in ensuring the tissue-wide sealing of the Casparian strip network and compare this to the situation in animal epithelia.

Selected Publications

Polarly localized kinase SGN1 is required for Casparian strip integrity and positioning.Alassimone J, Fujita S, Doblas VG, van Dop M, Barberon M, Kalmbach L, Vermeer JE, Rojas-Murcia N, Santuari L, Hardtke CS, Geldner N
Nat Plants 2016 Jul 25; 2:16113


Casparian strips are precisely localized and aligned ring-like cell wall modifications in the root of all higher plants. They set up an extracellular diffusion barrier analogous to animal tight junctions, and are crucial for maintaining the homeostatic capacity of plant roots. Casparian strips become localized because of the formation of a highly stable plasma membrane domain, consisting of a family of small transmembrane proteins called Casparian strip membrane domain proteins (CASPs). Here we report a large-scale forward genetic screen directly visualizing endodermal barrier function, which allowed us to identify factors required for the formation and integrity of Casparian strips. We present the identification and characterization of one of the mutants, schengen1 (sgn1), a receptor-like cytoplasmic kinase that we show localizes in a strictly polar fashion to the outer plasma membrane of endodermal cells and is required for the positioning and correct formation of the centrally located CASP domain.

Adaptation of Root Function by Nutrient-Induced Plasticity of Endodermal Differentiation.Barberon M, Vermeer JE, De Bellis D, Wang P, Naseer S, Andersen TG, Humbel BM, Nawrath C, Takano J, Salt DE, Geldner N
Cell 2016 Jan 28; 164(3):447-59


Plant roots forage the soil for minerals whose concentrations can be orders of magnitude away from those required for plant cell function. Selective uptake in multicellular organisms critically requires epithelia with extracellular diffusion barriers. In plants, such a barrier is provided by the endodermis and its Casparian strips--cell wall impregnations analogous to animal tight and adherens junctions. Interestingly, the endodermis undergoes secondary differentiation, becoming coated with hydrophobic suberin, presumably switching from an actively absorbing to a protective epithelium. Here, we show that suberization responds to a wide range of nutrient stresses, mediated by the stress hormones abscisic acid and ethylene. We reveal a striking ability of the root to not only regulate synthesis of suberin, but also selectively degrade it in response to ethylene. Finally, we demonstrate that changes in suberization constitute physiologically relevant, adaptive responses, pointing to a pivotal role of the endodermal membrane in nutrient homeostasis.

A receptor-like kinase mutant with absent endodermal diffusion barrier displays selective nutrient homeostasis defects.Pfister A, Barberon M, Alassimone J, Kalmbach L, Lee Y, Vermeer JE, Yamazaki M, Li G, Maurel C, Takano J, Kamiya T, Salt DE, Roppolo D, Geldner N
Elife 2014 Sep 16; 3:e03115


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.

A spatial accommodation by neighboring cells is required for organ initiation in Arabidopsis.Vermeer JE, von Wangenheim D, Barberon M, Lee Y, Stelzer EH, Maizel A, Geldner N
Science 2014 Jan 10; 343(6167):178-83


Lateral root formation in plants can be studied as the process of interaction between chemical signals and physical forces during development. Lateral root primordia grow through overlying cell layers that must accommodate this incursion. Here, we analyze responses of the endodermis, the immediate neighbor to an initiating lateral root. Endodermal cells overlying lateral root primordia lose volume, change shape, and relinquish their tight junction-like diffusion barrier to make way for the emerging lateral root primordium. Endodermal feedback is absolutely required for initiation and growth of lateral roots, and we provide evidence that this is mediated by controlled volume loss in the endodermis. We propose that turgidity and rigid cell walls, typical of plants, impose constraints that are specifically modified for a given developmental process.

A mechanism for localized lignin deposition in the endodermis.Lee Y, Rubio MC, Alassimone J, Geldner N
Cell 2013 Apr 11; 153(2):402-12


The precise localization of extracellular matrix and cell wall components is of critical importance for multicellular organisms. Lignin is a major cell wall modification that often forms intricate subcellular patterns that are central to cellular function. Yet the mechanisms of lignin polymerization and the subcellular precision of its formation remain enigmatic. Here, we show that the Casparian strip, a lignin-based, paracellular diffusion barrier in plants, forms as a precise, median ring by the concerted action of a specific, localized NADPH oxidase, brought into proximity of localized peroxidases through the action of Casparian strip domain proteins (CASPs). Our findings in Arabidopsis provide a simple mechanistic model of how plant cells regulate lignin formation with subcellular precision. We speculate that scaffolding of NADPH oxidases to the downstream targets of the reactive oxygen species (ROS) that they produce might be a widespread mechanism to ensure specificity and subcellular precision of ROS action within the extracellular matrix.

Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin.Naseer S, Lee Y, Lapierre C, Franke R, Nawrath C, Geldner N
Proc Natl Acad Sci U S A 2012 Jun 19; 109(25):10101-6


Casparian strips are ring-like cell-wall modifications in the root endodermis of vascular plants. Their presence generates a paracellular barrier, analogous to animal tight junctions, that is thought to be crucial for selective nutrient uptake, exclusion of pathogens, and many other processes. Despite their importance, the chemical nature of Casparian strips has remained a matter of debate, confounding further molecular analysis. Suberin, lignin, lignin-like polymers, or both, have been claimed to make up Casparian strips. Here we show that, in Arabidopsis, suberin is produced much too late to take part in Casparian strip formation. In addition, we have generated plants devoid of any detectable suberin, which still establish functional Casparian strips. In contrast, manipulating lignin biosynthesis abrogates Casparian strip formation. Finally, monolignol feeding and lignin-specific chemical analysis indicates the presence of archetypal lignin in Casparian strips. Our findings establish the chemical nature of the primary root-diffusion barrier in Arabidopsis and enable a mechanistic dissection of the formation of Casparian strips, which are an independent way of generating tight junctions in eukaryotes.

A novel protein family mediates Casparian strip formation in the endodermis.Roppolo D, De Rybel B, Dénervaud Tendon V, Pfister A, Alassimone J, Vermeer JE, Yamazaki M, Stierhof YD, Beeckman T, Geldner N
Nature 2011 May 19; 473(7347):380-3


Polarized epithelia are fundamental to multicellular life. In animal epithelia, conserved junctional complexes establish membrane diffusion barriers, cellular adherence and sealing of the extracellular space. Plant cellular barriers are of independent evolutionary origin. The root endodermis strongly resembles a polarized epithelium and functions in nutrient uptake and stress resistance. Its defining features are the Casparian strips, belts of specialized cell wall material that generate an extracellular diffusion barrier. 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.