IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45925-5.html
   My bibliography  Save this article

Dynamic root microbiome sustains soybean productivity under unbalanced fertilization

Author

Listed:
  • Mingxing Wang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • An-Hui Ge

    (Chinese Academy of Sciences)

  • Xingzhu Ma

    (Heilongjiang Academy of Black Soil Conservation and Utilization)

  • Xiaolin Wang

    (South China Agricultural University)

  • Qiujin Xie

    (Chinese Academy of Sciences)

  • Like Wang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Xianwei Song

    (Chinese Academy of Sciences)

  • Mengchen Jiang

    (Chinese Academy of Sciences)

  • Weibing Yang

    (Chinese Academy of Sciences)

  • Jeremy D. Murray

    (Chinese Academy of Sciences)

  • Yayu Wang

    (Ministry of Agriculture, BGI Research)

  • Huan Liu

    (Ministry of Agriculture, BGI Research
    Northeast Forestry University)

  • Xiaofeng Cao

    (Chinese Academy of Sciences)

  • Ertao Wang

    (Chinese Academy of Sciences
    ShanghaiTech University)

Abstract

Root-associated microbiomes contribute to plant growth and health, and are dynamically affected by plant development and changes in the soil environment. However, how different fertilizer regimes affect quantitative changes in microbial assembly to effect plant growth remains obscure. Here, we explore the temporal dynamics of the root-associated bacteria of soybean using quantitative microbiome profiling (QMP) to examine its response to unbalanced fertilizer treatments (i.e., lacking either N, P or K) and its role in sustaining plant growth after four decades of unbalanced fertilization. We show that the root-associated bacteria exhibit strong succession during plant development, and bacterial loads largely increase at later stages, particularly for Bacteroidetes. Unbalanced fertilization has a significant effect on the assembly of the soybean rhizosphere bacteria, and in the absence of N fertilizer the bacterial community diverges from that of fertilized plants, while lacking P fertilizer impedes the total load and turnover of rhizosphere bacteria. Importantly, a SynCom derived from the low-nitrogen-enriched cluster is capable of stimulating plant growth, corresponding with the stabilized soybean productivity in the absence of N fertilizer. These findings provide new insights in the quantitative dynamics of the root-associated microbiome and highlight a key ecological cluster with prospects for sustainable agricultural management.

Suggested Citation

  • Mingxing Wang & An-Hui Ge & Xingzhu Ma & Xiaolin Wang & Qiujin Xie & Like Wang & Xianwei Song & Mengchen Jiang & Weibing Yang & Jeremy D. Murray & Yayu Wang & Huan Liu & Xiaofeng Cao & Ertao Wang, 2024. "Dynamic root microbiome sustains soybean productivity under unbalanced fertilization," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45925-5
    DOI: 10.1038/s41467-024-45925-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45925-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-45925-5?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Yang Bai & Daniel B. Müller & Girish Srinivas & Ruben Garrido-Oter & Eva Potthoff & Matthias Rott & Nina Dombrowski & Philipp C. Münch & Stijn Spaepen & Mitja Remus-Emsermann & Bruno Hüttel & Alice C., 2015. "Functional overlap of the Arabidopsis leaf and root microbiota," Nature, Nature, vol. 528(7582), pages 364-369, December.
    2. Mengting Maggie Yuan & Xue Guo & Linwei Wu & Ya Zhang & Naijia Xiao & Daliang Ning & Zhou Shi & Xishu Zhou & Liyou Wu & Yunfeng Yang & James M. Tiedje & Jizhong Zhou, 2021. "Climate warming enhances microbial network complexity and stability," Nature Climate Change, Nature, vol. 11(4), pages 343-348, April.
    3. L. F. Schulte-Uebbing & A. H. W. Beusen & A. F. Bouwman & W. de Vries, 2022. "From planetary to regional boundaries for agricultural nitrogen pollution," Nature, Nature, vol. 610(7932), pages 507-512, October.
    4. Ning Ling & Tingting Wang & Yakov Kuzyakov, 2022. "Rhizosphere bacteriome structure and functions," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    5. Tianjiao Dai & Donghui Wen & Colin T. Bates & Linwei Wu & Xue Guo & Suo Liu & Yifan Su & Jiesi Lei & Jizhong Zhou & Yunfeng Yang, 2022. "Nutrient supply controls the linkage between species abundance and ecological interactions in marine bacterial communities," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    6. Davide Bulgarelli & Matthias Rott & Klaus Schlaeppi & Emiel Ver Loren van Themaat & Nahal Ahmadinejad & Federica Assenza & Philipp Rauf & Bruno Huettel & Richard Reinhardt & Elmon Schmelzer & Joerg Pe, 2012. "Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota," Nature, Nature, vol. 488(7409), pages 91-95, August.
    7. Feiyun Xu & Hanpeng Liao & Jinyong Yang & Yingjiao Zhang & Peng Yu & Yiying Cao & Ju Fang & Shu Chen & Liang Li & Leyun Sun & Chongxuan Du & Ke Wang & Xiaolin Dang & Zhiwei Feng & Yifan Cao & Ying Li , 2023. "Auxin-producing bacteria promote barley rhizosheath formation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Yuxiang Zhao & Zishu Liu & Baofeng Zhang & Jingjie Cai & Xiangwu Yao & Meng Zhang & Ye Deng & Baolan Hu, 2023. "Inter-bacterial mutualism promoted by public goods in a system characterized by deterministic temperature variation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Zhaohui Cao & Wenlong Zuo & Lanxiang Wang & Junyu Chen & Zepeng Qu & Fan Jin & Lei Dai, 2023. "Spatial profiling of microbial communities by sequential FISH with error-robust encoding," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Lige Ma & Yu Luo & Chen Chen & Huan Luo & Shuqi Wang & Yue Yuan & Wenhua Yang & Can Liu & Xulv Cao & Nannan Li, 2023. "Bacterial Strategies for Improving the Yield, Quality, and Adaptability of Oil Crops," Agriculture, MDPI, vol. 14(1), pages 1-29, December.
    4. Ke Tao & Ib T. Jensen & Sha Zhang & Eber Villa-Rodríguez & Zuzana Blahovska & Camilla Lind Salomonsen & Anna Martyn & Þuríður Nótt Björgvinsdóttir & Simon Kelly & Luc Janss & Marianne Glasius & Rasmus, 2024. "Nitrogen and Nod factor signaling determine Lotus japonicus root exudate composition and bacterial assembly," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    5. Carmen Escudero-Martinez & Max Coulter & Rodrigo Alegria Terrazas & Alexandre Foito & Rumana Kapadia & Laura Pietrangelo & Mauro Maver & Rajiv Sharma & Alessio Aprile & Jenny Morris & Pete E. Hedley &, 2022. "Identifying plant genes shaping microbiota composition in the barley rhizosphere," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. Feiyun Xu & Hanpeng Liao & Jinyong Yang & Yingjiao Zhang & Peng Yu & Yiying Cao & Ju Fang & Shu Chen & Liang Li & Leyun Sun & Chongxuan Du & Ke Wang & Xiaolin Dang & Zhiwei Feng & Yifan Cao & Ying Li , 2023. "Auxin-producing bacteria promote barley rhizosheath formation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    7. Dongnan Huang & Han Zheng & Jing Cheng & Guanxiong Wu & Lei Zheng & En Xie, 2023. "Nitrogen and Phosphorus Discriminate the Assembly Processes of Prokaryotic and Eukaryotic Algae in an Agricultural Drainage Receiving Lake," Sustainability, MDPI, vol. 15(3), pages 1-18, January.
    8. Shikai La & Jiafan Li & Si Ma & Xingqun Liu & Lihong Gao & Yongqiang Tian, 2024. "Protective role of native root-associated bacterial consortium against root-knot nematode infection in susceptible plants," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    9. Hao Zhang & Zi-Wei Hua & Wen-Zhi Liang & Qiu-Hong Niu & Xiang Wang, 2020. "The Prevention of Bio-Organic Fertilizer Fermented from Cow Manure Compost by Bacillus sp. XG-1 on Watermelon Continuous Cropping Barrier," IJERPH, MDPI, vol. 17(16), pages 1-16, August.
    10. Chenyan Sha & Zhixiong Wang & Jiajie Cao & Jing Chen & Cheng Shen & Jing Zhang & Qiang Wang & Min Wang, 2024. "Management of Spartina alterniflora : Assessing the Efficacy of Plant Growth Regulators on Ecological and Microbial Dynamics," Sustainability, MDPI, vol. 16(17), pages 1-14, September.
    11. Rita Biasi & Elena Brunori & Silvia Vanino & Alessandra Bernardini & Alessia Catalani & Roberta Farina & Antonio Bruno & Gabriele Chilosi, 2023. "Soil–Plant Interaction Mediated by Indigenous AMF in Grafted and Own-Rooted Grapevines under Field Conditions," Agriculture, MDPI, vol. 13(5), pages 1-13, May.
    12. Xin Zhou & Jinting Wang & Fang Liu & Junmin Liang & Peng Zhao & Clement K. M. Tsui & Lei Cai, 2022. "Cross-kingdom synthetic microbiota supports tomato suppression of Fusarium wilt disease," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    13. Lucas Hemmerle & Benjamin A. Maier & Miriam Bortfeld-Miller & Birgitta Ryback & Christoph G. Gäbelein & Martin Ackermann & Julia A. Vorholt, 2022. "Dynamic character displacement among a pair of bacterial phyllosphere commensals in situ," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    14. Benjamin H. Good & Layton B. Rosenfeld, 2023. "Eco-evolutionary feedbacks in the human gut microbiome," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    15. Tian, Lixin & Yang, Yu & Song, Youhong & Feng, Baili, 2024. "Rehydration under extreme drought conditions affected rhizosphere microorganisms more than bulk soil in broomcorn millet farmland," Agricultural Water Management, Elsevier, vol. 295(C).
    16. Xuanyu Tao & Zhifeng Yang & Jiajie Feng & Siyang Jian & Yunfeng Yang & Colin T. Bates & Gangsheng Wang & Xue Guo & Daliang Ning & Megan L. Kempher & Xiao Jun A. Liu & Yang Ouyang & Shun Han & Linwei W, 2024. "Experimental warming accelerates positive soil priming in a temperate grassland ecosystem," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    17. Löw, Philipp & Osterburg, Bernhard, 2024. "Evaluation of nitrogen balances and nitrogen use efficiencies on farm level of the German agricultural sector," Agricultural Systems, Elsevier, vol. 213(C).
    18. Barbara Emmenegger & Julien Massoni & Christine M. Pestalozzi & Miriam Bortfeld-Miller & Benjamin A. Maier & Julia A. Vorholt, 2023. "Identifying microbiota community patterns important for plant protection using synthetic communities and machine learning," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    19. Li Fan & Katja Fröhlich & Eric Melzer & Rory N. Pruitt & Isabell Albert & Lisha Zhang & Anna Joe & Chenlei Hua & Yanyue Song & Markus Albert & Sang-Tae Kim & Detlef Weigel & Cyril Zipfel & Eunyoung Ch, 2022. "Genotyping-by-sequencing-based identification of Arabidopsis pattern recognition receptor RLP32 recognizing proteobacterial translation initiation factor IF1," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    20. Zeyu Xing & Li Wang & Debin Fang, 2023. "Unraveling the dynamics and identifying the “superstars” of R&D alliances in IUR collaboration: a two-mode network analysis in China," Palgrave Communications, Palgrave Macmillan, vol. 10(1), pages 1-19, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45925-5. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.