Modulation of Phosphate Deficiency-Induced Metabolic Changes by Iron Availability in Arabidopsis thaliana.

Ranju Chutia,Sarah Scharfenberg,Jörg Ziegler,Steffen Abel,Steffen Neumann

doi:10.3390/ijms22147609

Abstract

Concurrent suboptimal supply of several nutrients requires the coordination of nutrient-specific transcriptional, phenotypic, and metabolic changes in plants in order to optimize growth and development in most agricultural and natural ecosystems. Phosphate (Pi) and iron (Fe) deficiency induce overlapping but mostly opposing transcriptional and root growth responses in Arabidopsis thaliana. On the metabolite level, Pi deficiency negatively modulates Fe deficiency-induced coumarin accumulation, which is controlled by Fe as well as Pi deficiency response regulators. Here, we report the impact of Fe availability on seedling growth under Pi limiting conditions and on Pi deficiency-induced accumulation of amino acids and organic acids, which play important roles in Pi use efficiency. Fe deficiency in Pi replete conditions hardly changed growth and metabolite profiles in roots and shoots of Arabidopsis thaliana, but partially rescued growth under conditions of Pi starvation and severely modulated Pi deficiency-induced metabolic adjustments. Analysis of T-DNA insertion lines revealed the concerted coordination of metabolic profiles by regulators of Fe (FIT, bHLH104, BRUTUS, PYE) as well as of Pi (SPX1, PHR1, PHL1, bHLH32) starvation responses. The results show the interdependency of Pi and Fe availability and the interplay between Pi and Fe starvation signaling on the generation of plant metabolite profiles.

Highlights

Plant growth and development strongly depends on the availability of nutrients in agricultural and natural ecosystems
Pi deficiency leads to profound phenotypic changes such as decreased shoot weight and increased root to shoot ratios, which are accompanied by reprogramming of cellular metabolism, such as the substitution of phospholipids by sulfolipids or the hyper-accumulation of starch
We investigate shoot and root growth as well as metabolic changes in roots and shoots of Arabidopsis thaliana plants subjected to individual and combined Pi or roots and shoots of Arabidopsis thaliana plants subjected to individual and combined Pi

Summary

Introduction

Plant growth and development strongly depends on the availability of nutrients in agricultural and natural ecosystems. An increasing number of studies investigate the coordination of plant responses to nutrient ratios in order to elucidate the molecular components, which ensures optimal provision with all required nutrients under conditions of changing nutrient supply [1]. Phosphorus possesses crucial roles in energy and nucleotide metabolism and as a constituent of membranes. It is taken up by the plant in the form of inorganic phosphate (Pi , H2 PO4 − or HPO4 2− ) by epidermal and cortical cells of the roots and transferred to the xylem for translocation to the shoots, a process which is mediated by PHO 1 (PHOSPHATE1) in Arabidopsis thaliana [5,6,7]. Pi uptake is optimized by increased expression of root Pi transporters and increased exudation of Pi solubilizing compounds, such as phosphatases, to release Pi organically bound to the rhizosphere

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