Salicylic Acid Alleviates the Adverse Effects of Salt Stress in Torreya grandis cv. Merrillii Seedlings by Activating Photosynthesis and Enhancing Antioxidant Systems

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Abstract

Background

Salt stress is a major factor limiting plant growth and productivity. Salicylic acid (SA) has been shown to ameliorate the adverse effects of environmental stress on plants. To investigate the protective role of SA in ameliorating salt stress on Torreya grandis ( T. grandis) trees, a pot experiment was conducted to analyze the biomass, relative water content (RWC), chlorophyll content, net photosynthesis (Pn), gas exchange parameters, relative leakage conductivity (REC), malondialdehyde (MDA) content, and activities of superoxide dismutase (SOD) and peroxidase (POD) of T. grandis under 0.2% and 0.4% NaCl conditions with and without SA.

Methodology/Principal Findings

The exposure of T. grandis seedlings to salt conditions resulted in reduced growth rates, which were associated with decreases in RWC and Pn and increases in REC and MDA content. The foliar application of SA effectively increased the chlorophyll (chl (a+b)) content, RWC, net CO ₂ assimilation rates (Pn), and proline content, enhanced the activities of SOD, CAT and POD, and minimized the increases in the REC and MDA content. These changes increased the capacity of T. grandis in acclimating to salt stress and thus increased the shoot and root dry matter. However, when the plants were under 0% and 0.2% NaCl stress, the dry mass of the shoots and roots did not differ significantly between SA-treated plants and control plants.

Conclusions

SA induced the salt tolerance and increased the biomass of T. grandis cv. by enhancing the chlorophyll content and activity of antioxidative enzymes, activating the photosynthetic process, and alleviating membrane injury. A better understanding about the effect of salt stress in T. grandis is vital, in order gain knowledge over expanding the plantations to various regions and also for the recovery of T. grandis species in the future.

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Most cited references 12

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Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants.

D. W. LAWLOR, G. Cornic (2002)

Experimental studies on CO2 assimilation of mesophytic C3 plants in relation to relative water content (RWC) are discussed. Decreasing RWC slows the actual rate of photosynthetic CO2 assimilation (A) and decreases the potential rate (Apot). Generally, as RWC falls from c. 100 to c. 75%, the stomatal conductance (gs) decreases, and with it A. However, there are two general types of relation of Apot to RWC, which are called Type 1 and Type 2. Type 1 has two main phases. As RWC decreases from 100 to c. 75%, Apot is unaffected, but decreasing stomatal conductance (gs) results in smaller A, and lower CO2 concentration inside the leaf (Ci) and in the chloroplast (Cc), the latter falling possibly to the compensation point. Down-regulation of electron transport occurs by energy quenching mechanisms, and changes in carbohydrate and nitrogen metabolism are considered acclimatory, caused by low Ci and reversible by elevated CO2. Below 75% RWC, there is metabolic inhibition of Apot, inhibition of A then being partly (but progressively less) reversible by elevated CO2; gs regulates A progressively less, and Ci and CO2 compensation point, Gamma rise. It is suggested that this is the true stress phase, where the decrease in Apot is caused by decreased ATP synthesis and a consequent decreased synthesis of RuBP. In the Type 2 response, Apot decreases progressively at RWC 100 to 75%, with A being progressively less restored to the unstressed value by elevated CO2. Decreased gs leads to a lower Ci and Cc but they probably do not reach compensation point: gs becomes progressively less important and metabolic limitations more important as RWC falls. The primary effect of low RWC on Apot is most probably caused by limited RuBP synthesis, as a result of decreased ATP synthesis, either through inhibition of Coupling Factor activity or amount due to increased ion concentration. Carbohydrate synthesis and accumulation decrease. Type 2 response is considered equivalent to Type 1 at RWC below c. 75%, with Apot inhibited by limited ATP and RuBP synthesis, respiratory metabolism dominates and Ci and Gamma rise. The importance of inhibited ATP synthesis as a primary cause of decreasing Apot is discussed. Factors determining the Type 1 and Type 2 responses are unknown. Electron transport is maintained (but down-regulated) in Types 1 and 2 over a wide range of RWC, and a large reduced/oxidized adenylate ratio results. Metabolic imbalance results in amino acid accumulation and decreased and altered protein synthesis. These conditions profoundly affect cell functions and ultimately cause cell death. Type 1 and 2 responses may reflect differences in gs and in sensitivity of metabolism to decreasing RWC.

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Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings.

O Borsani, V Valpuesta, Luisa M Botella (2001)

Previous studies have shown that salicylic acid (SA) is an essential component of the plant resistance to pathogens. We now show that SA plays a role in the plant response to adverse environmental conditions, such as salt and osmotic stresses. We have studied the responses of wild-type Arabidopsis and an SA-deficient transgenic line expressing a salicylate hydroxylase (NahG) gene to different abiotic stress conditions. Wild-type plants germinated under moderate light conditions in media supplemented with 100 mM NaCl or 270 mM mannitol showed extensive necrosis in the shoot. In contrast, NahG plants germinated under the same conditions remained green and developed true leaves. The lack of necrosis observed in NahG seedlings under the same conditions suggests that SA potentiates the generation of reactive oxygen species in photosynthetic tissues during salt and osmotic stresses. This hypothesis is supported by the following observations. First, the herbicide methyl viologen, a generator of superoxide radical during photosynthesis, produced a necrotic phenotype only in wild-type plants. Second, the presence of reactive oxygen-scavenging compounds in the germination media reversed the wild-type necrotic phenotype seen under salt and osmotic stress. Third, a greater increase in the oxidized state of the glutathione pool under NaCl stress was observed in wild-type seedlings compared with NahG seedlings. Fourth, greater oxidative damage occurred in wild-type seedlings compared with NahG seedlings under NaCl stress as measured by lipid peroxidation. Our data support a model for SA potentiating the stress response of the germinating Arabidopsis seedling.

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Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity.

I. E. Bagci, Figen Eraslan, Nuray Cicek … (2007)

It has been proposed that salicylic acid (SA) acts as an endogenous signal molecule responsible for inducing abiotic stress tolerance in plants. The effect of varying salicylic acid (SA) supply (0, 0.1, 0.5 and 1.0mM) on growth, mineral uptake, membrane permeability, lipid peroxidation, H(2)O(2) concentration, UV-absorbing substances, chlorophyll and carotenoid concentrations of NaCl (40 mM) stressed maize (Zea mays L.) was investigated. Exogenously applied SA increased plant growth significantly both in saline and non-saline conditions. As a consequence of salinity stress, lipid peroxidation, measured in terms of malondialdehyde (MDA) content and membrane permeability was decreased by SA. UV-absorbing substances (UVAS) and H(2)O(2) concentration were increased by increasing levels of SA. SA also strongly inhibited Na(+) and Cl(-) accumulation, but stimulated N, Mg, Fe, Mn and Cu concentrations of salt stressed maize plants. These results suggest that SA could be used as a potential growth regulator to improve plant salinity stress resistance.

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Author and article information

Contributors

Jin-Song Zhang: 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: 2014

Publication date (Electronic): 10 October 2014

Volume: 9

Issue: 10

Electronic Location Identifier: e109492

Affiliations

[1 ]Nurturing Station for the State Key Laboratory of Subtropical Silviculture, Zhejiang A & F University, Lin’an, Hangzhou, P. R. China

[2 ]School of Forestry & Biotechnology, Zhejiang A & F University, Lin’an, Hangzhou, P. R. China

[3 ]China National Bamboo Research Center, Hangzhou, P. R. China

Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, China

Author notes

* E-mail: wujs@ 123456zafu.edu.cn

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

Conceived and designed the experiments: JSW. Performed the experiments: TTL YYH XHD HT CHS. Analyzed the data: TTL YYH. Contributed reagents/materials/analysis tools: TTL YYH JSW. Wrote the paper: TTL YYH JSW.

Article

Publisher ID: PONE-D-14-20055

DOI: 10.1371/journal.pone.0109492

PMC ID: 4193794

PubMed ID: 25302987

SO-VID: 36f6590e-6e37-44e9-b33f-384c70492191

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 : 15 May 2014

Date accepted : 1 September 2014

Page count

Pages: 9

Funding

This project was supported in part by the Fruit Innovation Team Project of Zhejiang Province (2009R50033-7) and the Major Project of National Spark Plan of China (2012GA700001). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Data Availability The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper.

Salicylic Acid Alleviates the Adverse Effects of Salt Stress in Torreya grandis cv. Merrillii Seedlings by Activating Photosynthesis and Enhancing Antioxidant Systems

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PLOS: COVID-19 pandemic

Most cited references 12

Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants.

Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings.

Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity.

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