Non-targeted profiling of semi-polar metabolites in Arabidopsis root exudates uncovers a role for coumarin secretion and lignification during the local response to phosphate limitation.

Jörg Ziegler,Stephan Schmidt,Jens Müller,Steffen Abel,Ranju Chutia,Nadine Strehmel,Dierk Scheel,Christoph Böttcher

doi:10.1093/jxb/erv539

Abstract

Plants have evolved two major strategies to cope with phosphate (Pi) limitation. The systemic response, mainly comprising increased Pi uptake and metabolic adjustments for more efficient Pi use, and the local response, enabling plants to explore Pi-rich soil patches by reorganization of the root system architecture. Unlike previous reports, this study focused on root exudation controlled by the local response to Pi deficiency. To approach this, a hydroponic system separating the local and systemic responses was developed. Arabidopsis thaliana genotypes exhibiting distinct sensitivities to Pi deficiency could be clearly distinguished by their root exudate composition as determined by non-targeted reversed-phase ultraperformance liquid chromatography electrospray ionization quadrupole-time-of-flight mass spectrometry metabolite profiling. Compared with wild-type plants or insensitive low phosphate root 1 and 2 (lpr1 lpr2) double mutant plants, the hypersensitive phosphate deficiency response 2 (pdr2) mutant exhibited a reduced number of differential features in root exudates after Pi starvation, suggesting the involvement of PDR2-encoded P5-type ATPase in root exudation. Identification and analysis of coumarins revealed common and antagonistic regulatory pathways between Pi and Fe deficiency-induced coumarin secretion. The accumulation of oligolignols in root exudates after Pi deficiency was inversely correlated with Pi starvation-induced lignification at the root tips. The strongest oligolignol accumulation in root exudates was observed for the insensitive lpr1 lpr2 double mutant, which was accompanied by the absence of Pi deficiency-induced lignin deposition, suggesting a role of LPR ferroxidases in lignin polymerization during Pi starvation.

Highlights

Soils may contain high amounts of the element phosphorus, the concentration of soluble, inorganic phosphate (Pi) is rather low in the rhizosphere
The strongest oligolignol accumulation in root exudates was observed for the insensitive lpr1 lpr2 double mutant, which was accompanied by the absence of Pi deficiency-induced lignin deposition, suggesting a role of LPR ferroxidases in lignin polymerization during Pi starvation
Lpr1 lpr2 double-mutant plants are insensitive to low Pi, which is manifested by similar primary root growth under +Pi and –Pi conditions (Svistoonoff et al, 2007)

Summary

Introduction

Soils may contain high amounts of the element phosphorus, the concentration of soluble, inorganic phosphate (Pi) is rather low in the rhizosphere. Under Pi deficiency, plants such as Arabidopsis thaliana develop more lateral roots and root hairs at higher density This reorganization is accompanied by the arrest of root growth at the primary root tip (LópezBucio et al, 2002; Ward et al, 2008; Abel, 2011; Péret et al, 2011; Müller et al, 2015). This developmental plasticity enables the plant to better explore Pi-enriched soil patches in otherwise Pi-deplete soils. The pdr and lpr lpr mutants are largely but oppositely affected in the local root growth response to Pi limitation

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