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Salicylic Acid Confers Salt Tolerance in Giant Juncao Through Modulation of Redox Homeostasis, Ionic Flux, and Bioactive Compounds: An Ionomics and Metabolomic Perspective of Induced Tolerance Responses

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Abstract

We investigated the stimulatory and/or inhibitory role of exogenous SA in alleviating the salt stress (250, 500 mM NaCl) in Pennisetum giganteum (Giant Juncao) through coordinated induction of redox homeostasis, ionic flux, and bioactive compounds. Salt stress radically impaired root and shoot (growth, fresh, and dry biomass as well as tolerance indices), leaf relative water content, and leaf chlorophyll a/b ratio of Juncao due to higher Na+ and Cl− accumulation followed by H2O2 generation, lipid peroxidation (MDA contents), and electrolyte leakage. However, the innate defense response of Juncao counteracted salt-induced damages by osmolytes accumulation combined with orchestrating antioxidants and ionic homeostasis mechanisms. Furthermore, the application of SA had an incremental impact on the development and productivity of high-salinity-exposed Juncao plants by increasing root length, plant biomass, tolerance indices, chlorophyll a/b ratio, and protein contents. Furthermore, SA treatment considerably decreased Na+ and Cl− toxicity by orchestrating antioxidant enzymes, ion transport, and secondary metabolism. Notably, the application of SA substantially mitigated the adverse effects of high salinity concentration (500 mM NaCl), owing to the simultaneous upregulation in enzymatic and non-enzymatic antioxidants, nutrient ion flux, alongside chlorogenic acid production. Thus, we concluded that SA enhanced the tolerance capability of Juncao plants in a NaCl concentration-dependent manner. The findings of this study will enable environmentalists and pharmacologists to gain dual farm-level benefits, including animal therapeutics and restoration of salinized soils for arable purposes.

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Acknowledgements

The authors are thankful to all the anonymous reviewers, research team, and funding agencies.

Funding

This work was supported by the National Key Research and Development Program [2016YFD0800807], National Nature Science Foundations of China [31702003, 31902105], Young Elite Scientists Sponsorship Program by CAST [2017QNRC001], Project funded by China Postdoctoral Science Foundation [2019M651505], Sponsored by “Chenguang Program” supported by Shanghai Education Development Foundation and Shanghai Municipal Education Commission [17CG07], Shanghai Agriculture Science and Technology Development Project [2018-4-13], Shanghai Municipal Science and Technology Commission Project [20dz1204804].

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Author notes

  1. Co-first author: Yuanfei Zhou.

Authors and Affiliations

  1. School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, 200240, People’s Republic of China

    Kashif Hayat, Yuanfei Zhou, Saiqa Menhas & Pei Zhou

  2. Key Laboratory of Urban Agriculture, Ministry of Agriculture and Rural Affairs, Shanghai, China

    Kashif Hayat, Yuanfei Zhou, Saiqa Menhas & Pei Zhou

  3. College of Landscape Architecture, Nanjing Forestry University, Nanjing, People’s Republic of China

    Sikandar Hayat

  4. Department of Botany, Plant Physiology Section, Aligarh Muslim University, Aligarh, 202002, India

    Tariq Aftab

  5. Doctoral Program in Science, Technology, Environment, and Mathematics. Department of Earth and Environmental Sciences, National Chung Cheng University, 168 University Rd., Min-Hsiung, Chiayi County, 62102, Taiwan

    Jochen Bundschuh

  6. School of Civil Engineering and Surveying, University of Southern Queensland, West Street, Toowoomba, QLD, 4350, Australia

    Jochen Bundschuh

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  1. Kashif Hayat
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  2. Yuanfei Zhou
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  3. Saiqa Menhas
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  4. Sikandar Hayat
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  7. Pei Zhou
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Contributions

KH: investigation, data curation, formal and software analysis, writing—original draft. YZ: methodology, project administration. SM: data curation, writing—review and editing. SH, JB, TA: writing—review and editing. PZ: conceptualization, funding acquisition.

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Correspondence to Pei Zhou.

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Hayat, K., Zhou, Y., Menhas, S. et al. Salicylic Acid Confers Salt Tolerance in Giant Juncao Through Modulation of Redox Homeostasis, Ionic Flux, and Bioactive Compounds: An Ionomics and Metabolomic Perspective of Induced Tolerance Responses. J Plant Growth Regul 41, 1999–2019 (2022). https://doi.org/10.1007/s00344-022-10581-w

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