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Arbuscular mycorrhiza augments aluminum tolerance in white clover (Trifolium repens L.) by strengthening the ascorbate–glutathione cycle and phosphorus acquisition

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Abstract

The ascorbate–glutathione (AsA–GSH) cycle is essential for detoxifying reactive oxygen species (ROS) under environmental stresses. The toxicity of aluminum (Al) limits the growth and performance of cultivated plants in acidic soil. However, there is limited information available on the relationship between arbuscular mycorrhizal symbiosis and the AsA-GSH cycle in host plants under Al stress. This study aimed to examine the impact of arbuscular mycorrhizal fungi (AMF), specifically Funneliformis mosseae, on the growth, antioxidant enzymes, components of the AsA-GSH cycle, and stress response gene expressions in white clover (Trifolium repens L.) under Al stress. Our findings demonstrate that AMF inoculation significantly reduced Al accumulation and increased phosphorus (P) content in the roots of white clover, thereby promoting plant biomass accumulation and mycorrhizal colonization under Al stress. AMF effectively scavenged Al-induced ROS (H2O2 and O2) by enhancing the activities of antioxidant enzymes, including superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT), as well as the components of the AsA-GSH cycle (e.g., enzymes and antioxidants) in the leaves and roots of white clover plants. Additionally, the mitigating effect of AMF was associated with the upregulation of genes involved in P transport (PHO1-2 and PHT1-7), the AsA-GSH pathway (GST-2 and APX-2), and Al stress (ALMT1) in white clover roots compared to control plants. Principal component analysis revealed that 65.9% of the total variance was explained by the first principal component. Dry mass showed a positive correlation with POD and P content, while exhibiting a highly negative correlation with ROS, antioxidant physiology index, Al content, and the expression of related genes in white clover. Overall, this study suggests that AMF enhances the tolerance of white clover to Al stress by improving P uptake and strengthening the AsA-GSH cycle.

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Acknowledgements

We thank the editor and reviewers for their valuable suggestions on the manuscript.

Funding

The work was supported by the University Natural Science Research Project of Anhui Province (YJS20210138), and Education Department Project of Zhejiang Province (Y202248486), Biodiversity Survey and Assessment Project of Ministry of Ecology and Environment in China (2019HJ2096001006).

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JY Writing-original draft. JL Reviewing, and Editing, Funding acquisition. Investigation, Methodology; YW Reviewing; YP visualization; GY Methodology, Conceptualization, Reviewing, and Editing. ZJ Reviewing and Editing, Funding acquisition. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Guo Yang.

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Wu, J., Luo, J., Wang, Y. et al. Arbuscular mycorrhiza augments aluminum tolerance in white clover (Trifolium repens L.) by strengthening the ascorbate–glutathione cycle and phosphorus acquisition. Physiol Mol Biol Plants 29, 1647–1661 (2023). https://doi.org/10.1007/s12298-023-01369-7

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  • DOI: https://doi.org/10.1007/s12298-023-01369-7

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