Abstract

Iron (Fe) is an essential microelement but is highly toxic when in excess. The response of plant roots to Fe toxicity and the nature of the regulatory pathways engaged are poorly understood. Here, we examined the response to excess Fe exposure in Arabidopsis wild type and ethylene mutants with a focus on primary root growth and the role of ethylene. We showed that excess Fe arrested primary root growth by decreasing both cell elongation and division, and principally resulteds from direct external Fe contact at the root tip. Pronounced ethylene, but not abscisic acid, evolution was associated with excess Fe exposure. Ethylene antagonists intensified root growth inhibition in the wild type, while the inhibition was significantly reduced in ethylene-overproduction mutants. We showed that ethylene plays a positive role in tissue Fe homeostasis, even in the absence of iron-plaque formation. Ethylene reduced Fe concentrations in the stele, xylem, and shoot. Furthermore, ethylene increased the expression of genes encoding Fe-sequestering ferritins. Additionally, ethylene significantly enhanced root K(+) status and upregulated K(+)-transporter (HAK5) expression. Our findings highlight the important role of ethylene in tissue Fe and K homeostasis and primary root growth under Fe stress in Arabidopsis.

Highlights

  • Iron (Fe) is an essential element for plants, but excessive presence of this element in soils and subsequent toxicity is common, especially in acidic and water-logged soils (Connolly and Guerinot, 2002)

  • The key chemical reactions proceeding intracellularly, and leading to oxidative tissue damage, are known as the Fenton reactions, which proceed in two steps, each leading to the production of strong oxidants, and, in turn, setting the stage for ‘run-away’ oxidative chain reactions: Abbreviations: ABA, abscisic acid; ACC, 1-aminocyclopropane-1-carboxylic acid; ACO, ACC oxidase; ACS, ACC synthase; Al, aluminium; ANOVA, analysis of variance; AOA, amino-oxyacetic acid; AVG, aminoethoxyvinylglycine; EDX, energy-dispersive X-ray; Fe, iron; FLU, fluridone; ICP-AES, inductively coupled plasma atomic emission spectroscopy; K, potassium; QC, quiescent centre; Quantitative real-time reverse transcription PCR (qRT-PCR), quantitative real-time reverse transcription-PCR; SE, standard error; SEM, scanning electron microscopy; WT, wild type

  • Root-tip contact with excess Fe is essential for inhibition of Arabidopsis primary root growth

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Summary

Introduction

Iron (Fe) is an essential element for plants, but excessive presence of this element in soils and subsequent toxicity is common, especially in acidic and water-logged soils (Connolly and Guerinot, 2002). Yield reductions of 10–100% have been reported in the case of the world’s leading crop species, rice, and Fe toxicity is considered one of the most formidable research and management challenges in rice cultivation (Becker and Asch, 2005). It has been recorded in other important crops such as wheat (Khabaz-Saberi et al, 2010, 2012). The key chemical reactions proceeding intracellularly, and leading to oxidative tissue damage, are known as the Fenton reactions, which proceed in two steps, each leading to the production of strong oxidants, and, in turn, setting the stage for ‘run-away’ oxidative chain reactions: Abbreviations: ABA, abscisic acid; ACC, 1-aminocyclopropane-1-carboxylic acid; ACO, ACC oxidase; ACS, ACC synthase; Al, aluminium; ANOVA, analysis of variance; AOA, amino-oxyacetic acid; AVG, aminoethoxyvinylglycine; EDX, energy-dispersive X-ray; Fe, iron; FLU, fluridone; ICP-AES, inductively coupled plasma atomic emission spectroscopy; K, potassium; QC, quiescent centre; qRT-PCR, quantitative real-time reverse transcription-PCR; SE, standard error; SEM, scanning electron microscopy; WT, wild type

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