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Plant Physiol. 2017 Jul;174(3):1648-1668. doi: 10.1104/pp.16.01916. Epub 2017 May 12.

Heavy Metals Induce Iron Deficiency Responses at Different Hierarchic and Regulatory Levels.

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Department of Physiology and Cell Biology, Leibniz Institute for Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany.
Department of Environmental Ecology, Faculty of Natural Sciences, Comenius University in Bratislava, 84215 Bratislava, Slovakia.
Department of Plant Physiology, Plant Science and Biodiversity Center, Slovak Academy of Sciences, 84523 Bratislava, Slovakia.
Department of Physiology and Cell Biology, Leibniz Institute for Plant Genetics and Crop Plant Research, 06466 Gatersleben, Germany


In plants, the excess of several heavy metals mimics iron (Fe) deficiency-induced chlorosis, indicating a disturbance in Fe homeostasis. To examine the level at which heavy metals interfere with Fe deficiency responses, we carried out an in-depth characterization of Fe-related physiological, regulatory, and morphological responses in Arabidopsis (Arabidopsis thaliana) exposed to heavy metals. Enhanced zinc (Zn) uptake closely mimicked Fe deficiency by leading to low chlorophyll but high ferric-chelate reductase activity and coumarin release. These responses were not caused by Zn-inhibited Fe uptake via IRON-REGULATED TRANSPORTER (IRT1). Instead, Zn simulated the transcriptional response of typical Fe-regulated genes, indicating that Zn affects Fe homeostasis at the level of Fe sensing. Excess supplies of cobalt and nickel altered root traits in a different way from Fe deficiency, inducing only transient Fe deficiency responses, which were characterized by a lack of induction of the ethylene pathway. Cadmium showed a rather inconsistent influence on Fe deficiency responses at multiple levels. By contrast, manganese evoked weak Fe deficiency responses in wild-type plants but strongly exacerbated chlorosis in irt1 plants, indicating that manganese antagonized Fe mainly at the level of transport. These results show that the investigated heavy metals modulate Fe deficiency responses at different hierarchic and regulatory levels and that the interaction of metals with physiological and morphological Fe deficiency responses is uncoupled. Thus, this study not only emphasizes the importance of assessing heavy metal toxicities at multiple levels but also provides a new perspective on how Fe deficiency contributes to the toxic action of individual heavy metals.

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