A Novel Signaling Pathway Required for Arabidopsis Endodermal Root Organization Shapes the Rhizosphere Microbiome.

Julius Durr,Hugh G Dickinson,Jose Gutierrez-Marcos,Cathal Meehan,Paulina Flis,Umashankar Shivshankar,Sally Hilton,David Salt,Takehiro Kamiya,Gary D Bending,Shruti Pavagadhi,Wu Qi,Attila Feher,Sanjay Swarup,Guilhem Reyt,Stijn Spaepen

doi:10.1093/pcp/pcaa170

Abstract

The Casparian strip (CS) constitutes a physical diffusion barrier to water and nutrients in plant roots, which is formed by the polar deposition of lignin polymer in the endodermis tissue. The precise pattern of lignin deposition is determined by the scaffolding activity of membrane-bound Casparian Strip domain proteins (CASPs), but little is known of the mechanism(s) directing this process. Here, we demonstrate that Endodermis-specific Receptor-like Kinase 1 (ERK1) and, to a lesser extent, ROP Binding Kinase1 (RBK1) are also involved in regulating CS formation, with the former playing an essential role in lignin deposition as well as in the localization of CASP1. We show that ERK1 is localized to the cytoplasm and nucleus of the endodermis and that together with the circadian clock regulator, Time for Coffee (TIC), forms part of a novel signaling pathway necessary for correct CS organization and suberization of the endodermis, with their single or combined loss of function resulting in altered root microbiome composition. In addition, we found that other mutants displaying defects in suberin deposition at the CS also display altered root exudates and microbiome composition. Thus, our work reveals a complex network of signaling factors operating within the root endodermis that establish both the CS diffusion barrier and influence the microbial composition of the rhizosphere.

Highlights

Plant roots are specialized structures essential for plant growth and survival
To identify novel components of the signaling pathway implicated in the formation of the Casparian strip (CS), we carried out an in silico analysis of receptor-like kinases (RLK) that are under the control of MYB36—a transcription factor implicated in endodermis gene expression and CS formation (Kamiya et al 2015)
We investigated the expression of the closest homologue of Endodermis-specific Receptor-like Kinase 1 (ERK1), ROP binding kinase1 (RBK1), and found that it was largely restricted to the root endodermis (Supplementary Fig. S1B)

Summary

Introduction

Roots control the selective uptake of nutrients and water from the soil, and prevent the passive diffusion and entry of pathogens and toxins (Hawes et al 1998, Parniske 2008), while attracting beneficial microorganisms through the secretion of certain compounds into the soil (Sasse et al 2018). This selectivity is determined by the root architecture and its ability to confer a barrier between the vascular cylinder and the outer cell layers, primarily cortex and epidermis, which are connected to the soil via the apoplast to control the uptake and the exudation of compounds. Suberization of the CS shows high plasticity in contrast to lignification of the CS

Methods

Results

Conclusion