H2 Enhances Arabidopsis Salt Tolerance by Manipulating ZAT10/12-Mediated Antioxidant Defence and Controlling Sodium Exclusion

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Abstract

Background

The metabolism of hydrogen gas (H ₂) in bacteria and algae has been extensively studied for the interesting of developing H ₂-based fuel. Recently, H ₂ is recognized as a therapeutic antioxidant and activates several signalling pathways in clinical trials. However, underlying physiological roles and mechanisms of H ₂ in plants as well as its signalling cascade remain unknown.

Methodology/Principal Findings

In this report, histochemical, molecular, immunological and genetic approaches were applied to characterize the participation of H ₂ in enhancing Arabidopsis salt tolerance. An increase of endogenous H ₂ release was observed 6 hr after exposure to 150 mM NaCl. Arabidopsis pretreated with 50% H ₂-saturated liquid medium, mimicking the induction of endogenous H ₂ release when subsequently exposed to NaCl, effectively decreased salinity-induced growth inhibition. Further results showed that H ₂ pretreatment modulated genes/proteins of zinc-finger transcription factor ZAT10/12 and related antioxidant defence enzymes, thus significantly counteracting the NaCl-induced reactive oxygen species (ROS) overproduction and lipid peroxidation. Additionally, H ₂ pretreatment maintained ion homeostasis by regulating the antiporters and H ⁺ pump responsible for Na ⁺ exclusion (in particular) and compartmentation. Genetic evidence suggested that SOS1 and cAPX1 might be the target genes of H ₂ signalling.

Conclusions

Overall, our findings indicate that H ₂ acts as a novel and cytoprotective regulator in coupling ZAT10/12-mediated antioxidant defence and maintenance of ion homeostasis in the improvement of Arabidopsis salt tolerance.

Related collections

Most cited references 30

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In Arabidopsis thaliana, the SOS1 (Salt Overly Sensitive 1) locus is essential for Na(+) and K(+) homeostasis, and sos1 mutations render plants more sensitive to growth inhibition by high Na(+) and low K(+) environments. SOS1 is cloned and predicted to encode a 127-kDa protein with 12 transmembrane domains in the N-terminal part and a long hydrophilic cytoplasmic tail in the C-terminal part. The transmembrane region of SOS1 has significant sequence similarities to plasma membrane Na(+)/H(+) antiporters from bacteria and fungi. Sequence analysis of various sos1 mutant alleles reveals several residues and regions in the transmembrane as well as the tail parts that are critical for SOS1 function in plant salt tolerance. SOS1 gene expression in plants is up-regulated in response to NaCl stress. This up-regulation is abated in sos3 or sos2 mutant plants, suggesting that it is controlled by the SOS3/SOS2 regulatory pathway.

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Author and article information

Contributors

Miguel A. Blazquez: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2012

Publication date (Electronic): 21 November 2012

Volume: 7

Issue: 11

Electronic Location Identifier: e49800

Affiliations

[1 ]College of Life Sciences, Co. Laboratory of Nanjing Agricultural University, Nanjing, Jiangsu Province, China

[2 ]Carl Zeiss Far East, Nanjing Agricultural University, Nanjing, Jiangsu Province, China

Instituto de Biología Molecular y Celular de Plantas, Spain

Author notes

* E-mail: wbshenh@ 123456njau.edu.cn

Competing Interests: The authors have declared that no competing interests exist.

Conceived and designed the experiments: YX YM WS. Performed the experiments: YX YM DL WZ. Analyzed the data: YX YM WS. Contributed reagents/materials/analysis tools: YX WS. Wrote the paper: YX WS.

Article

Publisher ID: PONE-D-12-20969

DOI: 10.1371/journal.pone.0049800

PMC ID: 3504229

PubMed ID: 23185443

SO-VID: 3e0b3052-6316-4ff6-8904-9b21b363f71e

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 13 July 2012

Date accepted : 12 October 2012

Page count

Pages: 11

Funding

This work was supported by the National Natural Science Foundation of China (grant no. 31170241), the Education Department of Jiangsu (grant no. 200910), and the Fundamental Research Funds for the Central Universities (grant no. KYZ200905). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.