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Trehalose pretreatment induces salt tolerance in rice (Oryza sativa L.) seedlings: oxidative damage and co-induction of antioxidant defense and glyoxalase systems

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Abstract

Salinity in the form of abiotic stress adversely effects plant growth, development, and productivity. Various osmoprotectants are involved in regulating plant responses to salinity; however, the precise role of trehalose (Tre) in this process remains to be further elucidated. The present study investigated the regulatory role of Tre in alleviating salt-induced oxidative stress in hydroponically grown rice seedlings. Salt stress (150 and 250 mM NaCl) for 72 h resulted in toxicity symptoms such as stunted growth, severe yellowing, and leaf rolling, particularly at 250 mM NaCl. Histochemical observation of reactive oxygen species (ROS; O2 ∙− and H2O2) indicated evident oxidative stress in salt-stressed seedlings. In these seedlings, the levels of lipoxygenase (LOX) activity, malondialdehyde (MDA), H2O2, and proline (Pro) increased significantly whereas total chlorophyll (Chl) and relative water content (RWC) decreased. Salt stress caused an imbalance in non-enzymatic antioxidants, i.e., ascorbic acid (AsA) content, AsA/DHA ratio, and GSH/GSSG ratio decreased but glutathione (GSH) content increased significantly. In contrast, Tre pretreatment (10 mM, 48 h) significantly addressed salt-induced toxicity symptoms and dramatically depressed LOX activity, ROS, MDA, and Pro accumulation whereas AsA, GSH, RWC, Chl contents, and redox status improved considerably. Salt stress stimulated the activities of SOD, GPX, APX, MDHAR, DHAR, and GR but decreased the activities of CAT and GST. However, Tre-pretreated salt-stressed seedlings counteracted SOD and MDHAR activities, elevated CAT and GST activities, further enhanced APX and DHAR activities, and maintained GPX and GR activities similar to the seedlings stressed with salt alone. In addition, Tre pretreatment enhanced the activities of methylglyoxal detoxifying enzymes (Gly I and Gly II) more efficiently in salt-stressed seedlings. Our results suggest a role for Tre in protecting against salt-induced oxidative damage attributed to reduced ROS accumulation, elevation of non-enzymatic antioxidants, and co-activation of the antioxidative and glyoxalase systems.

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Abbreviations

AsA:

Ascorbic acid

CAT:

Catalase

Chl:

Chlorophyll

DHA:

Dehydroascorbate

Gly:

Glyoxalase

GR:

Glutathione reductase

GSH:

Reduced glutathione

GSSG:

Oxidized glutathione

H2O2 :

Hydrogen peroxide

LOX:

Lipoxygenase

MDA:

Malondialdehyde

MG:

Methylglyoxal

O2 .− :

Superoxide

Pro:

Proline

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

Tre:

Trehalose

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Acknowledgments

M.G. Mostofa gratefully acknowledges the funding from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Laboratory of Plant Stress Responses, Department of Applied Biological Science, Faculty of Agriculture, Kagawa University, Miki, Kagawa, 761-0795, Japan

    Mohammad Golam Mostofa & Masayuki Fujita

  2. Department of Biochemistry and Molecular Biology, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, 1706, Bangladesh

    Mohammad Golam Mostofa

  3. Department of Genetics and Plant Breeding, Bangladesh Agricultural University, Mymensingh, 2202, Bangladesh

    Mohammad Anwar Hossain

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  1. Mohammad Golam Mostofa
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  2. Mohammad Anwar Hossain
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  3. Masayuki Fujita
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Correspondence to Masayuki Fujita.

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Supplementary table 1

Summary of the effect of trehalose on the components of oxidative stress, non-enzymatic, enzymatic, and glyoxalase systems in rice seedlings under salt stress. Tre, S1, Tre+S1, S2, and Tre+S2 correspond to 10 mM trehalose, 150 mM NaCl, 10 mM trehalose + 150 mM NaCl, 250 mM NaCl, and 10 mM trehalose + 250 mM NaCl, respectively (PDF 133 kb)

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Mostofa, M.G., Hossain, M.A. & Fujita, M. Trehalose pretreatment induces salt tolerance in rice (Oryza sativa L.) seedlings: oxidative damage and co-induction of antioxidant defense and glyoxalase systems. Protoplasma 252, 461–475 (2015). https://doi.org/10.1007/s00709-014-0691-3

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