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Mycorrhizosphere bacteria inhibit chromium uptake and phytotoxicity by regulating proline metabolism, antioxidant defense system, and aquaporin gene expression in tomato

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Abstract

Chromium (Cr) contamination in soil–plant systems poses a pressing environmental challenge due to its detrimental impacts on plant growth and human health. Results exhibited that Cr stress decreased shoot biomass, root biomass, leaf relative water content, and plant height. However, single and co-application of Bacillus subtilis (BS) and arbuscular mycorrhizal fungi (AMF) considerably enhanced shoot biomass (+ 21%), root biomass (+ 2%), leaf relative water content (+ 26%), and plant height (+ 13) under Cr stress. The frequency of mycorrhizal (F) association (+ 5%), mycorrhizal colonization (+ 13%), and abundance of arbuscules (+ 5%) in the non-stressed soil was enhanced when inoculated with combined BS and AMF as compared to Cr-stressed soil. The co-inoculation with BS and AMF considerably enhanced total chlorophyll, carotenoids, and proline content in Cr-stressed plants. Cr-stressed plants resulted in attenuated response in SOD, POD, CAT, and GR activities when inoculated with BS and AMF consortia by altering oxidative stress biomarkers (H2O2 and MDA). In Cr-stressed plants, the combined application of BS and AMF considerably enhanced proline metabolism, for instance, P5CR (+ 17%), P5CS (+ 28%), OAT (− 22%), and ProDH (− 113%) as compared to control. Sole inoculation with AMF downregulated the expression of SIPIP2;1, SIPIP2;5, and SIPIP2;7 in Cr-stressed plants. However, the expression of NCED1 was downregulated with the application of sole AMF. In contrast, the relative expression of Le4 was upregulated in the presence of AMF and BS combination in Cr-stressed plants. Therefore, it is concluded that co-application of BS and AMF enhanced Cr tolerance by enhancing proline metabolism, antioxidant enzymes, and aquaporin gene expression. Future study might concentrate on elucidating the molecular processes behind the synergistic benefits of BS and AMF, as well as affirming their effectiveness in field experiments under a variety of environmental situations. Long-term research on the effect of microbial inoculation on soil health and plant production might also help to design sustainable chromium remediation solutions.

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Funding

This project was supported by Researchers Supporting Project number (RSP2024R230) King Saud University, Riyadh, Saudi Arabia.

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Authors and Affiliations

  1. Department of Agronomy, Faculty of Crop Production Sciences, The University of Agriculture, Peshawar, Peshawar, 25130, Pakistan

    Tariq Shah

  2. Department of Plant Biotechnology, Atta-ur-Rahman School of Applied Biosciences, National University of Sciences and Technology, Islamabad, 44000, Pakistan

    Zeeshan Khan, Ayesha Imran, Muhammad Asad & Shah Rukh Khan

  3. Department of Pediatrics, College of Medicine and King, Medical City, Khalid University Hospital, King Saud University, PO Box-2925, 11461, Riyadh, Saudi Arabia

    Tahani Awad Alahmadi

  4. Department of Botany, Hindu College, Moradabad, Mahatma Jyotiba Phule Rohilkhand University Bareilly, Moradabad, India

    Mohammad Javed Ansari

  5. College of Food and Agriculture Sciences, King Saud University, Riyadh, Saudi Arabia

    Mohammad Javed Ansari

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  1. Tariq Shah
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Contributions

All authors contributed to the study conception and design. Tariq Shah conceived and designed the experiment; Tariq Shah prepared the materials and data collection; M. Asad assisted in software and statistical analysis of the data; Zeeshan Khan wrote the first draft of the manuscript; Ayesha Imran assisted in the software used for graphical representation of data; S. Khan assisted in materials and reagents preparation; Tahani AA. assisted in review of manuscript and funding; Mohammad Javed Ansari assisted in review, editing, and approval of final version. All authors read and approved the final manuscript.

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Shah, T., Khan, Z., Alahmadi, T.A. et al. Mycorrhizosphere bacteria inhibit chromium uptake and phytotoxicity by regulating proline metabolism, antioxidant defense system, and aquaporin gene expression in tomato. Environ Sci Pollut Res 31, 24836–24850 (2024). https://doi.org/10.1007/s11356-024-32755-7

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