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Shoot to root communication is necessary to control the expression of iron-acquisition genes in Strategy I plants

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Abstract

Previous research showed that auxin, ethylene, and nitric oxide (NO) can activate the expression of iron (Fe)-acquisition genes in the roots of Strategy I plants grown with low levels of Fe, but not in plants grown with high levels of Fe. However, it is still an open question as to how Fe acts as an inhibitor and which pool of Fe (e.g., root, phloem, etc.) in the plant acts as the key regulator for gene expression control. To further clarify this, we studied the effect of the foliar application of Fe on the expression of Fe-acquisition genes in several Strategy I plants, including wild-type cultivars of Arabidopsis [Arabidopsis thaliana (L.) Heynh], pea [Pisum sativum L.], tomato [Solanum lycopersicon Mill.], and cucumber [Cucumis sativus L.], as well as mutants showing constitutive expression of Fe-acquisition genes when grown under Fe-sufficient conditions [Arabidopsis opt3-2 and frd3-3, pea dgl and brz, and tomato chln (chloronerva)]. The results showed that the foliar application of Fe blocked the expression of Fe-acquisition genes in the wild-type cultivars and in the frd3-3, brz, and chln mutants, but not in the opt3-2 and dgl mutants, probably affected in the transport of a Fe-related repressive signal in the phloem. Moreover, the addition of either ACC (ethylene precursor) or GSNO (NO donor) to Fe-deficient plants up-regulated the expression of Fe-acquisition genes, but this effect did not occur in Fe-deficient plants sprayed with foliar Fe, again suggesting the existence of a Fe-related repressive signal moving from leaves to roots.

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Abbreviations

ACC:

1-Aminocyclopropane-1-carboxylic acid

EDDHA:

N,N′-ethylenebis[2-(2-hydroxyphenyl)-glycine]

Ferrozine:

3-(2-Pyridyl)-5,6-bis(4-phenyl-sulfonic acid)-1,2,4-triazine

NA:

Nicotianamine

GSNO:

S-nitrosoglutathione

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Acknowledgments

We thank Dr Michael Grusak (USDA/ARS, Houston, Texas, USA), Dr Ross Welch (USDA/ARS, Ithaca, New York, USA), and Dr Petra Bauer (Saarland University, Saarbrücken, Germany) for kindly providing seeds of the Sparkle [dgl,dgl] mutant, the brz mutant, and the chloronerva mutant. We also thank the Arabidopsis Biological Resource Center (Ohio State University, USA) for providing seeds of the frd3-3 mutant. This work was supported by the European Regional Development Fund from the European Union, the “Ministerio de Educación y Ciencia” (Projects AGL2007-64372 and AGL2010-17121), and the “Junta de Andalucía” (Research Groups AGR115 and BIO159, and Project AGR-3849). Funding to MGS and GS was provided by a Grant from the USA National Science Foundation Plant Genome Program (Award #0820769).

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Authors and Affiliations

  1. Department of Agronomy, Edificio Celestino Mutis (C-4), Campus de Excelencia Internacional Agroalimentario de Rabanales (ceiA3), University of Córdoba, 14014, Córdoba, Spain

    Francisco J. Romera, Eduardo Villar & Esteban Alcántara

  2. Divisions of Plant Science and Biochemistry, University of Missouri, Columbia, MO, 65211, USA

    Minviluz G. Stacey & Gary Stacey

  3. Department of Botany, Ecology and Plant Physiology, Edificio Celestino Mutis (C-4), Campus de Rabanales, University of Córdoba, 14014, Córdoba, Spain

    María J. García & Rafael Pérez-Vicente

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  1. María J. García
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  2. Francisco J. Romera
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  3. Minviluz G. Stacey
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Correspondence to Francisco J. Romera.

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García, M.J., Romera, F.J., Stacey, M.G. et al. Shoot to root communication is necessary to control the expression of iron-acquisition genes in Strategy I plants. Planta 237, 65–75 (2013). https://doi.org/10.1007/s00425-012-1757-0

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