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  • Review Article
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Cross-kingdom nutrient exchange in the plant–arbuscular mycorrhizal fungus–bacterium continuum

Abstract

The association between plants and arbuscular mycorrhizal fungi (AMF) affects plant performance and ecosystem functioning. Recent studies have identified AMF-associated bacteria as cooperative partners that participate in AMF–plant symbiosis: specific endobacteria live inside AMF, and hyphospheric bacteria colonize the soil that surrounds the extraradical hyphae. In this Review, we describe the concept of a plant–AMF–bacterium continuum, summarize current advances and provide perspectives on soil microbiology. First, we review the top-down carbon flow and the bottom-up mineral flow (especially phosphorus and nitrogen) in this continuum, as well as how AMF–bacteria interactions influence the biogeochemical cycling of nutrients (for example, carbon, phosphorus and nitrogen). Second, we discuss how AMF interact with hyphospheric bacteria or endobacteria to regulate nutrient exchange between plants and AMF, and the possible molecular mechanisms that underpin this continuum. Finally, we explore future prospects for studies on the hyphosphere to facilitate the utilization of AMF and hyphospheric bacteria in sustainable agriculture.

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Fig. 1: An overview of the plant–arbuscular mycorrhizal fungus–bacterium continuum and the two key interfaces involved in nutrient exchange.
Fig. 2: Carbon and mineral flows in the plant–arbuscular mycorrhizal fungus–bacterium continuum.
Fig. 3: Molecular mechanisms regulating carbon and mineral exchange in the plant–arbuscular mycorrhizal fungus–bacterium continuum.
Fig. 4: The bacteria living inside the AMF cytoplasm.

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Acknowledgements

The authors are grateful to J. Mach for the critical reading of this manuscript, to N. Hofmann for the discussion on the ‘continuum’ term and to M. Novero for the assembly of Fig. 4. This work was financially supported by the National Natural Science Foundation of China (32130094, 32170116 and 42277112), Guangdong Basic and Applied Basic Research Foundation (2022A1515012013) and China Scholarship Council (202206350052).

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S.D., E.L., P.B., X.X. and L.Z. contributed substantially to the discussion of content and wrote the manuscript. S.D., G.F. and L.Z. discussed the original logic and framework of this manuscript. S.D., P.B., X.X. and L.Z. contributed literature searching for this manuscript and reviewed and edited the manuscript before submission.

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Correspondence to Paola Bonfante, Xianan Xie or Lin Zhang.

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Duan, S., Feng, G., Limpens, E. et al. Cross-kingdom nutrient exchange in the plant–arbuscular mycorrhizal fungus–bacterium continuum. Nat Rev Microbiol 22, 773–790 (2024). https://doi.org/10.1038/s41579-024-01073-7

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