Elemental Concentrations in the Seed of Mutants and Natural Variants of Arabidopsis thaliana Grown under Varying Soil Conditions

Stephen C Mcdowell,Chris Sladek,Nick Saini,Julian I Schroeder,David Mendoza-Cozatl,Joe B Morrissey,John M Ward,Mary Lou Guerinot,Jeffrey F Harper,David E Salt,Garo Akmakjian,Ivan Baxter,Ron Mittler

doi:10.1371/journal.pone.0063014

Abstract

The concentrations of mineral nutrients in seeds are critical to both the life cycle of plants as well as human nutrition. These concentrations are strongly influenced by soil conditions, as shown here by quantifying the concentration of 14 elements in seeds from Arabidopsis thaliana plants grown under four different soil conditions: standard, or modified with NaCl, heavy metals, or alkali. Each of the modified soils resulted in a unique change to the seed ionome (the mineral nutrient content of the seeds). To help identify the genetic networks regulating the seed ionome, changes in elemental concentrations were evaluated using mutants corresponding to 760 genes as well as 10 naturally occurring accessions. The frequency of ionomic phenotypes supports an estimate that as much as 11% of the A. thaliana genome encodes proteins of functional relevance to ion homeostasis in seeds. A subset of mutants were analyzed with two independent alleles, providing five examples of genes important for regulation of the seed ionome: SOS2, ABH1, CCC, At3g14280 and CNGC2. In a comparison of nine different accessions to a Col-0 reference, eight accessions were observed to have reproducible differences in elemental concentrations, seven of which were dependent on specific soil conditions. These results indicate that the A. thaliana seed ionome is distinct from the vegetative ionome, and that elemental analysis is a sensitive approach to identify genes controlling ion homeostasis, including those that regulate gene expression, phospho-regulation, and ion transport.

Highlights

Ion homeostasis is a complex process that is essential to the health and survival of all organisms
Soil Modifications Affect Ion Homeostasis in Col-0 Seed To evaluate the impact of growth conditions on the A. thaliana seed ionome, the concentration of 14 elements (Ba, Ca, Cd, Cu, Fe, K Li, Mg, Mn, Mo, Na, P, S and Zn) was quantified in the seed of plants grown under four different soil conditions: standard, or modified with NaCl (75 mM NaCl), heavy metals (Al, As, Cd, Co, Ba, Cs, Cr, Cu, Ca, Fe, Mn, Mg, Li, Rb), or alkali
NaCl conditions increased relative concentrations of K, Li and Na; heavy metal conditions increased Ca, Cd, Cu, and S, but decreased Fe and Mn; and alkali conditions increased Ca, Cu, K, and S, but decreased Ba and Fe. This indicated that the chosen conditions were sufficient to alter ion homeostasis in the seed, supporting an expectation that these conditions could be used in the context of a mutant screen to increase the probability of identifying mutations that alter ion accumulation in the seed

Summary

Introduction

Ion homeostasis is a complex process that is essential to the health and survival of all organisms. While at least 14 mineral nutrients are essential for higher plants [1], they can be toxic if present in excess. Most land plants obtain their mineral nutrients from the soil, with homeostasis involving the regulation of uptake, binding, transport and sequestration; each of which is controlled by a network of genes. Large scale screens to identify ionomic mutants have been undertaken in yeast, A. thaliana and Lotus [5,6,7,8]. These studies have provided estimates that approximately 5% of the genome might be involved in ion homeostasis. Ionomic techniques have been applied to crop plants including maize, rice, tomato and wheat [24,25,26,27]

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