Oxidative stress is a consequence, not a cause, of aluminum toxicity in the forage legume Lotus corniculatus

Authors

  • Joaquín Navascués,

    1. Departamento de Nutrición Vegetal, Estación Experimental de Aula Dei, Consejo Superior de Investigaciones Científicas, Apartado 13034, 50080 Zaragoza, Spain
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  • Carmen Pérez-Rontomé,

    1. Departamento de Nutrición Vegetal, Estación Experimental de Aula Dei, Consejo Superior de Investigaciones Científicas, Apartado 13034, 50080 Zaragoza, Spain
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  • Diego H. Sánchez,

    1. Max Planck Institute for Molecular Plant Physiology, Wissenschaftspark Golm, Am Mühlenberg 1, Potsdam-Golm, 14476, Germany
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  • Christiana Staudinger,

    1. Department of Molecular Systems Biology, University of Vienna, 1090 Vienna, Austria
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  • Stefanie Wienkoop,

    1. Department of Molecular Systems Biology, University of Vienna, 1090 Vienna, Austria
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  • Rubén Rellán-Álvarez,

    1. Departamento de Nutrición Vegetal, Estación Experimental de Aula Dei, Consejo Superior de Investigaciones Científicas, Apartado 13034, 50080 Zaragoza, Spain
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  • Manuel Becana

    1. Departamento de Nutrición Vegetal, Estación Experimental de Aula Dei, Consejo Superior de Investigaciones Científicas, Apartado 13034, 50080 Zaragoza, Spain
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Author for correspondence:
Manuel Becana
Tel: +34 976 716055
Email: becana@eead.csic.es

Summary

  • Aluminum (Al) toxicity is a major limiting factor of crop production on acid soils, but the implication of oxidative stress in this process is controversial. A multidisciplinary approach was used here to address this question in the forage legume Lotus corniculatus.
  • Plants were treated with low Al concentrations in hydroponic culture, and physiological and biochemical parameters, together with semiquantitative metabolic and proteomic profiles, were determined.
  • The exposure of plants to 10 μM Al inhibited root and leaf growth, but had no effect on the production of reactive oxygen species or lipid peroxides. By contrast, exposure to 20 μM Al elicited the production of superoxide radicals, peroxide and malondialdehyde. In response to Al, there was a progressive replacement of the superoxide dismutase isoforms in the cytosol, a loss of ascorbate and consistent changes in amino acids, sugars and associated enzymes.
  • We conclude that oxidative stress is not a causative factor of Al toxicity. The increased contents in roots of two powerful Al chelators, malic and 2-isopropylmalic acids, together with the induction of an Al-activated malate transporter gene, strongly suggest that both organic acids are implicated in Al detoxification. The effects of Al on key proteins involved in cytoskeleton dynamics, protein turnover, transport, methylation reactions, redox control and stress responses underscore a metabolic dysfunction, which affects multiple cellular compartments, particularly in plants exposed to 20 μM Al.

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