Skip to main content
SpringerLink
Log in

Phenomic profiling to reveal tolerance mechanisms and regulation of ascorbate–glutathione cycle in wheat varieties (Triticum aestivum L.) under arsenic stress

  • Original Paper
  • Published:
Environmental Geochemistry and Health Aims and scope Submit manuscript

Abstract

The potential of arsenic (As) tolerant and sensitive varieties of wheat (Triticum aestivum L.) has yet to be explored despite of alarming situation of arsenic toxicity. To fill this gap, the study aimed to explore the role of antioxidants, phytochelatins, and ascorbate–glutathione for As tolerance in wheat. A total of eight varieties were exposed to different arsenate treatments (0, 1, 5, 10, 50, 100, 200, 500, 1000, 2000, and 10,000 μM) initially to screen effective treatment as well as contrasting varieties via Weibull distribution frequency for further analysis. The Weibull analysis found 200 μM as the most effective treatment in the present study. Selected varieties were analyzed for accumulation of total As and As speciation, oxidative stress (malondialdehyde, hydrogen peroxide), antioxidants (superoxide dismutase, catalase, peroxidase), phytochelatins, and ascorbate–glutathione cycle (glutathione-S-transferase, glutathione reductase, glutathione peroxidase, ascorbate peroxidase). Tolerant varieties showed less accumulation and translocation of total As, arsenate, and arsenite to the shoots compared with sensitive varieties under 200 μM treatment. Low concentration in tolerant varieties correlated with better growth and development response. Tolerant varieties showed higher induction of metabolites (glutathione, phytochelatins) compared to sensitive ones. Furthermore, tolerant varieties showed better performance of antioxidant and ascorbate–glutathione cycle enzymes in response to As exposure. The findings of the present study provided great insight into the wheat tolerance mechanism upon As exposure between contrasting varieties.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abbas, G., Murtaza, B., Bibi, I., Shahid, M., Niazi, N. K., Khan, M. I., Amjad, M., Hussain, M., & Natasha,. (2018). Arsenic uptake, toxicity, detoxification, and speciation in plants: Physiological, biochemical, and molecular aspects. International Journal of Environmental Research and Public Health, 15(1), 59.

    Article  Google Scholar 

  • Aebi, H. (1984). [13] Catalase in vitro Methods in enzymology (Vol. 105, pp. 121–126): Elsevier.

  • Akram, N. A., Shafiq, F., & Ashraf, M. (2017). Ascorbic acid-a potential oxidant scavenger and its role in plant development and abiotic stress tolerance. Frontiers in Plant Science, 8, 613.

    Article  Google Scholar 

  • Aksakal, O., & Esim, N. (2015). Evaluation of arsenic trioxide genotoxicity in wheat seedlings using oxidative system and RAPD assays. Environmental Science and Pollution Research, 22(9), 7120–7128.

    Article  CAS  Google Scholar 

  • Alamri, S., Siddiqui, M. H., Mukherjee, S., Kumar, R., Kalaji, H. M., Irfan, M., Minkina, T., & Rajput, V. D. (2022). Molybdenum-induced endogenous nitric oxide (NO) signaling coordinately enhances resilience through chlorophyll metabolism, osmolyte accumulation and antioxidant system in arsenate stressed-wheat (Triticum aestivum L.) seedlings. Environmental Pollution, 292, 118268.

    Article  CAS  Google Scholar 

  • Ando, K., Honma, M., Chiba, S., Tahara, S., & Mizutani, J. (1988). Glutathione transferase from Mucor javamicus. Agricultural and Biological Chemistry, 52(1), 135–139.

    CAS  Google Scholar 

  • Asada, K. (1994). Mechanisms for scavenging reactive molecules generated in chloroplasts under light stress. Photoinhibition of photosynthesis from molecular mechanisms to the field., 129–142.

  • Beauchamp, C., & Fridovich, I. (1971). Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry, 44(1), 276–287.

    Article  CAS  Google Scholar 

  • Begum, M. C., Islam, M. S., Islam, M., Amin, R., Parvez, M. S., & Kabir, A. H. (2016). Biochemical and molecular responses underlying differential arsenic tolerance in rice (Oryza sativa L.). Plant Physiology and Biochemistry, 104, 266–277.

    Article  CAS  Google Scholar 

  • Bergmeyer, H.-U. (2012). Methods of enzymatic analysis. Elsevier.

    Google Scholar 

  • Bergqvist, C., & Greger, M. (2012). Arsenic accumulation and speciation in plants from different habitats. Applied Geochemistry, 27(3), 615–622.

    Article  CAS  Google Scholar 

  • Chowdhury, N. R., Das, R., Joardar, M., Ghosh, S., Bhowmick, S., & Roychowdhury, T. (2018). Arsenic accumulation in paddy plants at different phases of pre-monsoon cultivation. Chemosphere, 210, 987–997.

    Article  CAS  Google Scholar 

  • Dago, A., Ariño, C., Díaz-Cruz, J. M., & Esteban, M. (2014). Analysis of phytochelatins and Hg-phytochelatin complexes in Hordeum vulgare plants stressed with Hg and Cd: HPLC study with amperometric detection. International Journal of Environmental Analytical Chemistry, 94(7), 668–678.

    Article  CAS  Google Scholar 

  • Das, S., Majumder, B., & Biswas, A. K. (2018). Modulation of growth, ascorbate-glutathione cycle and thiol metabolism in rice (Oryza sativa L. cv. MTU-1010) seedlings by arsenic and silicon. Ecotoxicology, 27(10), 1387–1403.

    Article  CAS  Google Scholar 

  • Drotar, A., Phelps, P., & Fall, R. (1985). Evidence for glutathione peroxidase activities in cultured plant cells. Plant Science, 42(1), 35–40.

    Article  CAS  Google Scholar 

  • Fadhel, D. H. (2012). Spectrophotometric determination of ascorbic acid in aqueous solutions. Al-Nahrain Journal of Science, 15(3), 88–94.

    Google Scholar 

  • Greger, M., Kabir, A. H., Landberg, T., Maity, P. J., & Lindberg, S. (2016). Silicate reduces cadmium uptake into cells of wheat. Environmental Pollution, 211, 90–97.

    Article  CAS  Google Scholar 

  • Hasanuzzaman, M., Nahar, K., Anee, T. I., & Fujita, M. (2017). Glutathione in plants: Biosynthesis and physiological role in environmental stress tolerance. Physiology and Molecular Biology of Plants, 23(2), 249–268.

    Article  CAS  Google Scholar 

  • Heath, R. L., & Packer, L. (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 125(1), 189–198.

    Article  CAS  Google Scholar 

  • Javed, A., Farooqi, A., Baig, Z. U., Ellis, T., & van Geen, A. (2020). Soil arsenic but not rice arsenic increasing with arsenic in irrigation water in the Punjab plains of Pakistan. Plant and Soil, 450(1), 601–611.

    Article  CAS  Google Scholar 

  • Kashyap, L., & Garg, N. (2018). Arsenic toxicity in crop plants: responses and remediation strategies Mechanisms of Arsenic Toxicity and Tolerance in Plants (pp. 129–169). Springer.

    Book  Google Scholar 

  • Kiany, T., Pishkar, L., Sartipnia, N., Iranbakhsh, A., & Barzin, G. (2022). Effects of silicon and titanium dioxide nanoparticles on arsenic accumulation, phytochelatin metabolism, and antioxidant system by rice under arsenic toxicity. Environmental Science and Pollution Research, 29(23), 34725–34737.

    Article  CAS  Google Scholar 

  • Lichtenthaler, H. K., & Wellburn, A. R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents: Portland Press Ltd.

  • Majumder, B., Das, S., Mukhopadhyay, S., & Biswas, A. K. (2019). Identification of arsenic-tolerant and arsenic-sensitive rice (Oryza sativa L.) cultivars on the basis of arsenic accumulation assisted stress perception, morpho-biochemical responses, and alteration in genomic template stability. Protoplasma, 256(1), 193–211.

    Article  CAS  Google Scholar 

  • Mallick, S., Kumar, N., Sinha, S., Dubey, A. K., Tripathi, R. D., & Srivastav, V. (2014). H2O2 pretreated rice seedlings specifically reduces arsenate not arsenite: Difference in nutrient uptake and antioxidant defense response in a contrasting pair of rice cultivars. Physiology and Molecular Biology of Plants, 20(4), 435–447.

    Article  CAS  Google Scholar 

  • Mallick, S., Sinam, G., & Sinha, S. (2011). Study on arsenate tolerant and sensitive cultivars of Zea mays L.: differential detoxification mechanism and effect on nutrients status. Ecotoxicology and environmental safety, 74(5), 1316–1324.

    Article  CAS  Google Scholar 

  • Marques, D. N., Gaziola, S. A., & Azevedo, R. A. (2021). Phytochelatins and their relationship with modulation of cadmium tolerance in plants. Handbook of Bioremediation (pp. 91–113). Academic Press.

    Chapter  Google Scholar 

  • Martínez-Castillo, J. I., Saldaña-Robles, A., & Ozuna, C. (2022). Arsenic stress in plants: A metabolomic perspective. Plant Stress, 3, 100055.

    Article  Google Scholar 

  • Nabi, A., Aftab, T., Masroor, M., Khan, A., & Naeem, M. (2022). Exogenous triacontanol provides tolerance against arsenic-induced toxicity by scavenging ROS and improving morphology and physiological activities of Mentha arvensis L. Environmental Pollution, 295, 118609.

    Article  CAS  Google Scholar 

  • Pourghasemian, N., Landberg, T., Ehsanzadeh, P., & Greger, M. (2019). Different response to Cd stress in domesticated and wild safflower (Carthamus spp.). Ecotoxicology and Environmental Safety, 171, 321–328.

    Article  CAS  Google Scholar 

  • Sadasivam, S. (1996). Biochemical methods: New age international.

  • Saeed, M., Quraishi, U. M., & Malik, R. N. (2022). Identification of arsenic-tolerant varieties and candidate genes of tolerance in spring wheat (Triticum aestivum L.). Chemosphere, 308, 136380.

    Article  CAS  Google Scholar 

  • Seregin, I. V., & Kozhevnikova, A. D. (2023). Phytochelatins: Sulfur-containing metal (loid)-chelating ligands in plants. International Journal of Molecular Sciences, 24(3), 2430.

    Article  CAS  Google Scholar 

  • Shi, G., Ma, H., Chen, Y., Liu, H., Song, G., Cai, Q., & Rengel, Z. (2019). Low arsenate influx rate and high phosphorus concentration in wheat (Triticum aestivum L.): A mechanism for arsenate tolerance in wheat plants. Chemosphere, 214, 94–102.

    Article  CAS  Google Scholar 

  • Shi, S., Wang, T., Chen, Z., Tang, Z., Wu, Z., Salt, D. E., Chao, D. Y., & Zhao, F. J. (2016). OsHAC1; 1 and OsHAC1; 2 function as arsenate reductases and regulate arsenic accumulation. Plant Physiology, 172(3), 1708–1719.

    Article  CAS  Google Scholar 

  • Sil, P., Das, P., & Biswas, A. K. (2020). Impact of exogenous silicate amendments on nitrogen metabolism in wheat seedlings subjected to arsenate stress. SILICON, 12, 535–545.

    Article  CAS  Google Scholar 

  • Singh, P., & P., Singh, R., Singh, V. P., & Prasad, S. M. (2016). Heavy metal tolerance in plants: Role of transcriptomics, proteomics, metabolomics, and ionomics. Frontiers in Plant Science, 6, 1143.

    Article  Google Scholar 

  • Smith, I. K., Vierheller, T. L., & Thorne, C. A. (1988). Assay of glutathione reductase in crude tissue homogenates using 5, 5′-dithiobis (2-nitrobenzoic acid). Analytical Biochemistry, 175(2), 408–413.

    Article  CAS  Google Scholar 

  • Sneller, F. E. C., van Heerwaarden, L. M., Koevoets, P. L., Vooijs, R., Schat, H., & Verkleij, J. A. (2000). Derivatization of Phytochelatins from Silene v ulgaris, induced upon exposure to arsenate and cadmium: Comparison of derivatization with Ellman’s reagent and monobromobimane. Journal of Agricultural and Food Chemistry, 48(9), 4014–4019.

    Article  CAS  Google Scholar 

  • Suman, S., Sharma, P. K., Siddique, A. B., Rahman, M. A., Kumar, R., Rahman, M. M., Bose, N., Singh, S. K., Ghosh, A. K., Matthews, H., & Mondal, D. (2020). Wheat is an emerging exposure route for arsenic in Bihar India. Science of the Total Environment, 703, 134774.

    Article  CAS  Google Scholar 

  • Taylor, G. J., Stadt, K. J., & Dale, M. R. (1992). Modelling the interactive effects of aluminum, cadmium, manganese, nickel and zinc stress using the Weibull frequency distribution. Environmental and Experimental Botany, 32(3), 281–293.

    Article  CAS  Google Scholar 

  • Tripathi, P., Tripathi, R. D., Singh, R. P., Dwivedi, S., Chakrabarty, D., Trivedi, P. K., & Adhikari, B. (2013). Arsenite tolerance in rice (Oryza sativa L.) involves coordinated role of metabolic pathways of thiols and amino acids. Environmental Science and Pollution Research, 20(2), 884–896.

    Article  CAS  Google Scholar 

  • Velikova, V., Yordanov, I., & Edreva, A. (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines. Plant Science, 151(1), 59–66.

    Article  CAS  Google Scholar 

  • Yadav, S. K., Ramanathan, A., Kumar, M., Chidambaram, S., Gautam, Y., & Tiwari, C. (2020). Assessment of arsenic and uranium co-occurrences in groundwater of central Gangetic Plain, Uttar Pradesh. India. Environmental Earth Sciences, 79(6), 1–14.

    Google Scholar 

Download references

Acknowledgements

The authors are grateful to the International Research Support Initiative Program (IRSIP), Higher Education Commission (HEC), Pakistan, for providing fellowship (IRSIP 49 BMS 31) in the completion of this work. The authors are also grateful to Dr. Edouard Pesquet from the DEEP Department, at Stockholm University, Sweden, for his valuable guidance during the GSH-PCs analysis.

Author information

Authors and Affiliations

  1. Environmental Biology and Ecotoxicology Laboratory, Department of Environmental Sciences, Faculty of Biological Sciences, Quaid-I-Azam University, Islamabad, 45320, Pakistan

    Muhammad Saeed & Riffat Naseem Malik

  2. Department of Plant Sciences, Faculty of Biological Sciences, Quaid-I-Azam University, Islamabad, 45320, Pakistan

    Umar Masood Quraishi

  3. Plant Metal Laboratory, Department of Ecology, Environment, and Plant Sciences (DEEP), Stockholm University, Stockholm, Sweden

    Tommy Landberg & Maria Greger

Authors
  1. Muhammad Saeed
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Umar Masood Quraishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tommy Landberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria Greger
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Riffat Naseem Malik
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MS was involved in investigation, writing—original draft, data curation, and formal analysis. UMQ assisted with methodology and conceptualization. TL provided technical assistance. MG was responsible for resources, methodology, reviewing and editing, and supervision. RNM participated in supervision, project administration, and writing—reviewing and editing.

Corresponding author

Correspondence to Riffat Naseem Malik.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest in the present study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 346 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saeed, M., Quraishi, U.M., Landberg, T. et al. Phenomic profiling to reveal tolerance mechanisms and regulation of ascorbate–glutathione cycle in wheat varieties (Triticum aestivum L.) under arsenic stress. Environ Geochem Health 46, 2 (2024). https://doi.org/10.1007/s10653-023-01784-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10653-023-01784-5

Keywords

Search

Navigation