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Promoting soil microbial-mediated suppressiveness against Fusarium wilt disease by the enrichment of specific fungal taxa via crop rotation

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Abstract

A pineapple-banana rotation was studied as a model system to investigate the potential emergence of a fungal-mediated disease-suppression in a soil highly infested with the pathogen Fusarium oxysporum causing the banana wilt disease. By using both field and pot experiments, the pineapple-banana rotation system resulted in a significant decrease of the pathogen number and next-stubble banana disease incidence (P < 0.05). This pathogen-suppression phenomenon was linked with detectable shifts in the soil resident fungal taxa tracked in the pineapple season. Most importantly, taxa affiliated with Talaromyces pinophilus and Clonostachys rossmaniae were found to be significantly enriched in the bulk soils due to the pineapple cultivation (P < 0.05). The taxon T. pinophilus was also significantly enriched in the rhizosphere of banana after the rotation (P < 0.05). Later, we used fungal isolation and pot inoculation to validate that both T. pinophilus and C. rossmaniae taxa are able to significantly decrease the pathogen number in the banana rhizosphere soil (P < 0.05), thus confirming their biocontrol effects suppressing the disease. Taken together, this study provides evidence on how crop rotation affects the resident soil microbiome and the development of disease suppressiveness. Besides, this study highlights the importance of understanding the dynamic changes in soil biology mediated by crop rotation and validates the mechanisms underpinning suppression toward promoting practical and directed manipulation of protective microbiomes in agroecosystems.

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Acknowledgements

We sincerely thank all those who have assisted us with any part of this paper and Hainan WanZhong Co., Ltd. for providing access to the experimental equipment and greenhouse facilities.

Funding

This work was supported by the National Natural Science Foundation of China (42090065 and 31972509), the Fundamental Research Funds for the Central Universities (KYXK202009 and KYXK202008), the Hainan Provincial Natural Science Foundation of China (320RC483), the Priority Academic Program Development of the Jiangsu Higher Education Institutions (PAPD), the 111 project (B12009), and the Innovative Research Team Development Plan of the Ministry of Education of China (IRT_17R56).

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Authors and Affiliations

  1. Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University, Nanjing, 210095, Jiangsu, People’s Republic of China

    Xianfu Yuan, Wu Xiong, Zongzhuan Shen, Rong Li & Qirong Shen

  2. The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, 210095, Jiangsu, People’s Republic of China

    Xianfu Yuan, Wu Xiong, Zongzhuan Shen, Rong Li & Qirong Shen

  3. Hainan Key Laboratory for Sustainable Utilization of Tropical Bio-Resources, College of Tropical Crops, Hainan University, Haikou, 570228, People’s Republic of China

    Beibei Wang, Shan Hong & Yunze Ruan

  4. Department of Plant Science, The Pennsylvania State University, University Park, PA, USA

    Francisco Dini-Andreote

  5. Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, USA

    Francisco Dini-Andreote

  6. College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, China

    Rong Li

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  1. Xianfu Yuan
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  3. Shan Hong
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  4. Wu Xiong
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  7. Rong Li
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  9. Francisco Dini-Andreote
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Contributions

The experiment was designed by Rong Li. All experiments were performed by Xianfu Yuan. Data collection, analysis, and writing were performed by Xianfu Yuan, Rong Li, and Francisco Dini-Andreote. Beibei Wang, Wu Xiong, Zongzhuan Shen, Yunze Ruan, Qirong Shen, Francisco Dini-Andreote, and Shan Hong contributed to the intellectual input and assistance to this study and manuscript preparation.

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Correspondence to Rong Li.

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Yuan, X., Wang, B., Hong, S. et al. Promoting soil microbial-mediated suppressiveness against Fusarium wilt disease by the enrichment of specific fungal taxa via crop rotation. Biol Fertil Soils 57, 1137–1153 (2021). https://doi.org/10.1007/s00374-021-01594-w

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