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Promotion of Arabidopsis immune responses by a rhizosphere fungus via supply of pipecolic acid to plants and selective augment of phytoalexins

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Abstract

The ascomycete insect pathogenic fungi such as Metarhizium species have been demonstrated with the abilities to form the rhizosphere or endophytic relationships with different plants for nutrient exchanges. In this study, after the evident infeasibility of bacterial disease development in the boxed sterile soils, we established a hydroponic system for the gnotobiotic growth of Arabidopsis thaliana with the wild-type and transgenic strain of Metarhizium robertsii. The transgenic fungus could produce a high amount of pipecolic acid (PIP), a pivotal plant-immune-stimulating metabolite. Fungal inoculation experiments showed that M. robertsii could form a non-selective rhizosphere relationship with Arabidopsis. Similar to the PIP uptake by plants after exogenous application, PIP level increased in Col-0 and could be detected in the PIP-non-producing Arabidopsis mutant (ald1) after fungal inoculations, indicating that plants can absorb the PIP produced by fungi. The transgenic fungal strain had a better efficacy than the wild type to defend plants against the bacterial pathogen and aphid attacks. Contrary to ald1, fmo1 plants could not be boosted to resist bacterial infection after treatments. After fungal inoculations, the phytoalexins camalexin and aliphatic glucosinolate were selectively increased in Arabidopsis via both PIP-dependent and -independent ways. This study unveils the potential mechanism of the fungus-mediated beneficial promotion of plant immunity against biological stresses. The data also highlight the added values of M. robertsii to plants beyond the direct suppression of insect pest populations.

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Acknowledgements

This work was supported by the Chinese Academy of Sciences (XDPB16, QYZDJ-SSW-SMC028) and the National Natural Science Foundation of China (32021001, 31530001). We thank Dr. Xiangzong Meng for the gift of pad3 seeds. We also thank Dr. Yining Liu for help with the LC-MS analysis.

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Authors and Affiliations

  1. Key Laboratory of Insect Developmental and Evolutionary Biology, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China

    Feifei Luo, Guirong Tang, Song Hong & Chengshu Wang

  2. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, 100049, China

    Song Hong & Chengshu Wang

  3. National key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China

    Tianyu Gong & Xiu-Fang Xin

  4. School of Life Science and Technology, ShanghaiTech University, Shanghai, 201210, China

    Chengshu Wang

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  1. Feifei Luo
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Luo, F., Tang, G., Hong, S. et al. Promotion of Arabidopsis immune responses by a rhizosphere fungus via supply of pipecolic acid to plants and selective augment of phytoalexins. Sci. China Life Sci. 66, 1119–1133 (2023). https://doi.org/10.1007/s11427-022-2238-8

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