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Soil organic phosphorus is mainly hydrolyzed via phosphatases from ectomycorrhiza-associated bacteria rather than ectomycorrhizal fungi

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Abstract

Background and aims

Mycorrhizal fungi-released phosphatases have long been claimed pivotal to mobilize soil organic phosphorus (P). We hypothesized that ectomycorrhizal (ECM) fungi, compared with their saprotrophic ancestors, evolved adaptive strategies to enhance the release of phosphatases to meet the P demand of ECM fungi and their host plants.

Methods

We analyzed genes potentially encoding secreted phosphatases in 103 fungal species, ECM fungi hyphae associated- and ectomycorrhizosphere phosphatase enzyme activities, and gene expression of Lactarius spp. and Laccaria bicolor fungi-secreted phosphatases during ECM formation. We also determined ectomycorrhizosphere abundance of bacterial phosphatase genes, and analyzed Pinus yunnanensis–Lactarius deliciosus ectomycorrhiza-associated P-mobilizing bacteria.

Results

We found that during transition from saprotrophy to ECM symbiosis, genes encoding fungal-secreted phosphatases did not manifest adaptive or convergent evolution. Among 10 genes potentially encoding secreted fungal phosphatases in Lactarius spp. and Laccaria bicolor, only two were up-regulated during ECM formation. Furthermore, unlike saprotrophic fungi, pure-cultured ECM fungi hyphae released very few or no phosphatases to the surroundings, while ECMs generally increased the phosphatase activities in the ectomycorrhizosphere under glasshouse conditions. Additionally, ECM-associated bacteria exhibited an increased abundance of P-cycling genes in the ectomycorrhizosphere under both glasshouse and field conditions. A substantial part of culturable bacteria from ECM tips hydrolyzed organic P and promoted fungal P acquisition.

Conclusion

We found no evidence for adaptive evolution of secreted phosphatases in ECM fungi; some ECM fungi may not even release phosphatases, and ECM-associated bacteria likely play a pivotal role in ECM-promoted organic P hydrolysis and plant P acquisition.

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Data availability

RNAseq raw data used in this study are available in the NCBI Sequence Read Archive (SRA), accession no. PRJNA961221.

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Acknowledgements

Sincere thanks to Francis M. Martin (INRAE-Nancy) for providing Laccaria bicolor S238N strains and valuable personal communications. This work was supported by Yunnan Fundamental Research Projects (grant NO.202101AU070080) and National Natural Science Foundation of China (31901204 and 32170302) to YW. We also thank Yunnan High Level Talent Introduction Plans to YW and XH. HL received funding from the Deputy Vice Chancellor (Research) at the University of Western Australia.

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Authors and Affiliations

  1. The Germplasm Bank of Wild Species & Yunnan Key Laboratory for Fungal Diversity and Green Development, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan, 650201, China

    Jing Yuan, Rui Yan, Xueqiong Zhang, Kai Su, Hui Liu, Xin Wei, Ran Wang, Lanlan Huang, Wei Liu, Xinhua He, Fuqiang Yu & Yanliang Wang

  2. College of Resources and Environment, Yunnan Agricultural University, Kunming, Yunnan, 650500, China

    Jing Yuan, Shanping Wan & Yi Zheng

  3. Centre of Excellence for Soil Biology, College of Resources and Environment, and Chongqing Key Laboratory of Plant Resource Conservation and Germplasm Innovation, School of Life Sciences, Southwest University, Chongqing, 400716, China

    Rui Yan & Xinhua He

  4. Yunnan University, Kunming, Yunnan, 650504, China

    Xueqiong Zhang

  5. University of Chinese Academy of Sciences, Beijing, 100049, China

    Kai Su & Xin Wei

  6. Guangxi Key Laboratory of Plant Conservation and Restoration Ecology in Karst Terrain, Guangxi Institute of Botany, Guangxi Zhuang Autonomous Region and Chinese Academy of Sciences, Guilin, Guangxi, 541006, China

    Nianwu Tang

  7. School of Biological Sciences, University of Western Australia, Perth, WA, 6009, Australia

    Hans Lambers & Xinhua He

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  1. Jing Yuan
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Correspondence to Hans Lambers, Yi Zheng, Xinhua He, Fuqiang Yu or Yanliang Wang.

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Jing Yuan, Rui Yan, and Xueqiong Zhang are co-first authors.

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Yuan, J., Yan, R., Zhang, X. et al. Soil organic phosphorus is mainly hydrolyzed via phosphatases from ectomycorrhiza-associated bacteria rather than ectomycorrhizal fungi. Plant Soil (2024). https://doi.org/10.1007/s11104-024-06649-z

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