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A comparative study of the early osmotic, ionic, redox and hormonal signaling response in leaves and roots of two halophytes and a glycophyte to salinity

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Abstract

Salt stress is one of the most important abiotic stress factors affecting plant growth and productivity in natural ecosystems. In this study, we aimed at determining possible differences between salt tolerant and salt sensitive species in early (within 72 h) salt stress response in leaves and roots. To this purpose, we subjected three Brassicaceae species, namely two halophytes—Cakile maritima and Thellungiella salsuginea—and a glycophyte—Arabidopsis thaliana— to short-term salt stress (400 mM NaCl). The results indicate that the halophytes showed a differential osmotic and ionic response together with an early and transient oxidative burst, which was characterized by enhanced hydrogen peroxide levels and subsequent activation of antioxidant defenses in both leaves and roots. In addition, the halophytes displayed enhanced accumulation of abscisic acid, jasmonic acid (JA) and ACC (aminocyclopropane-1-carboxylic acid, the precursor of ethylene) in leaves and roots, as compared to A. thaliana under salt stress. Moreover, the halophytes showed enhanced expression of ethylene response factor1 (ERF1), the convergence node of the JA and ethylene signaling pathways in both leaves and roots upon exposure to salt stress. In conclusion, we show that the halophytes C. maritima and T. salsuginea experience an early oxidative burst, improved antioxidant defenses and hormonal response not only in leaves but also in roots, in comparison to the glycophyte A. thaliana. This differential signaling response converging, at least in part, into increased ERF1 expression in both above- and underground tissues seems to underlay, at least in part, the enhanced tolerance of the two studied halophytes to salt stress.

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Abbreviations

ABA:

Abscisic acid

ACC:

Aminocyclopropane-1-carboxylic acid

DAB:

3,3′-diaminobenzidine tetrahydrochloride

ERF1 :

Ethylene response factor1

F v/F m :

Maximum quantum yield of the PSII

GSH:

Glutathione

GSSG:

Glutathione disulfide

JA:

Jasmonic acid

MDA:

Malondialdehyde

ROS:

Reactive oxygen species

RWC:

Relative water content

TBA:

Thiobarbituric acid

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Acknowledgments

We are very grateful to Andreas M. Fischer (Montana State University) for critical insights into the manuscript. S. M. B. was funded by the Generalitat de Catalunya (ICREA Academia prize). H. E. was funded by the Tunisian Ministry for High Education and Scientific Research (LR10CBBC02). We thank Prof. A. Savouré (Université Pierre and Marie Curie) for providing us with the T. salsuginea seeds.

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Authors and Affiliations

  1. Departament de Biologia Vegetal, Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain

    Hasna Ellouzi, Iker Hernández, Jana Cela, Maren Müller & Sergi Munné-Bosch

  2. Laboratoire des Plantes Extrêmophiles, Center of Biotechnology of Borj Cedria, Hammam-Lif, Tunisia

    Hasna Ellouzi, Karim Ben Hamed & Chedly Abdelly

  3. EA 2219 Géoarchitecture, UFR Sciences et Techniques, Université de Brest, 29238, Brest Cedex3, France

    Christian Magné

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  1. Hasna Ellouzi
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Correspondence to Sergi Munné-Bosch.

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Ellouzi, H., Hamed, K.B., Hernández, I. et al. A comparative study of the early osmotic, ionic, redox and hormonal signaling response in leaves and roots of two halophytes and a glycophyte to salinity. Planta 240, 1299–1317 (2014). https://doi.org/10.1007/s00425-014-2154-7

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