, Volume 28, Issue 6, pp 1693–1704 | Cite as

NH4 + induces antioxidant cellular machinery and provides resistance to salt stress in citrus plants

  • Emma Fernández-Crespo
  • Rocío Gómez-Pastor
  • Loredana Scalschi
  • Eugenio Llorens
  • Gemma CamañesEmail author
  • Pilar García-Agustín
Original Paper
Part of the following topical collections:
  1. Salinity


Key message

NH 4 + acts as a mild oxidative stressor, which triggers antioxidant cellular machinery and provide resistance to salinity.


NH4 + nutrition in Carrizo citrange (Citrus sinensis L. Osbeck × Poncirus trifoliata L) plants acts as an inducer of resistance against salinity conditions. NH4 + treatment triggers mild chronic stress that primes plant defence responses by stress imprinting and confers protection against subsequent salt stress. In this work, we studied the influence of NH4 + nutrition on antioxidant enzymatic activities and metabolites involved in detoxification of reactive oxygen species (ROS) to clarify their involvement in NH4 +-mediated salt resistance. Our results showed that NH4 + nutrition induces in citrus plants high levels of H2O2, strongly inhibits superoxide dismutase (SOD) and glutathione reductase (GR) activities, and leads to higher content of oxidised glutathione (GSSG) than in control plants in the absence of salt, thus providing evidence to confirm mild stress induced by NH4 + nutrition. However, upon salinity, plants grown with NH4 + (N-NH4 + plants) showed a reduction of H2O2 levels in parallel to an increase of catalase (CAT), SOD, and GR activities compared with the control plants. Moreover, N-NH4 + plants were able to keep high levels of reduced glutathione (GSH) upon salinity and were able to induce glutathione-S-transferase (GST) and phospholipid hydroperoxide glutathione peroxidise (PHGPx) mRNA accumulation. Based on this evidence, we confirm that sublethal concentrations of NH4 + might act as a mild oxidative stressor, which triggers antioxidant cellular machinery that can provide resistance to subsequent salt stress.


Ammonium nutrition Citrus Salinity ROS and SIMR 



Ascorbate peroxidase






Fresh weight


Glyceraldehyde-3-phosphate dehydrogenase


Glutathione reductase




Phospholipid hydroperoxide glutathione peroxidase


Reactive oxygen species


Stress induced morphogenetic response


Superoxide dismutase



This work was supported by Prometeo 2012/066. Loredana Scalschi is the recipient of a PhD fellowship from the Ministerio de Educación (Grant AP2008-01064). Eugenio Llorens is the recipient of a PhD fellowship from Pla de promoció de la investigació de la Universitat Jaume I (Ajudes predoctorals ref 2009/24). We thank Emilia Matallana (UV) for her corrections and suggestions.

Conflict of interest

The authors declare that they have no conflict of interest.


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Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Emma Fernández-Crespo
    • 1
  • Rocío Gómez-Pastor
    • 2
  • Loredana Scalschi
    • 1
  • Eugenio Llorens
    • 1
  • Gemma Camañes
    • 1
    Email author
  • Pilar García-Agustín
    • 1
  1. 1.Grupo de Bioquímica y Biotecnología, Área de Fisiología Vegetal, Departamento de Ciencias Agrarias y del Medio Natural, ESTCEUniversitat Jaume ICastellónSpain
  2. 2.Departamento de Bioquímica y Biología MolecularUniversitat de ValenciaValenciaSpain

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