IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-47773-9.html
   My bibliography  Save this article

Purines enrich root-associated Pseudomonas and improve wild soybean growth under salt stress

Author

Listed:
  • Yanfen Zheng

    (Tobacco Research Institute of Chinese Academy of Agricultural Sciences)

  • Xuwen Cao

    (Shandong University)

  • Yanan Zhou

    (Tobacco Research Institute of Chinese Academy of Agricultural Sciences
    College of Resources and Environment of Shandong Agricultural University)

  • Siqi Ma

    (Tobacco Research Institute of Chinese Academy of Agricultural Sciences)

  • Youqiang Wang

    (Tobacco Research Institute of Chinese Academy of Agricultural Sciences)

  • Zhe Li

    (Tobacco Research Institute of Chinese Academy of Agricultural Sciences)

  • Donglin Zhao

    (Tobacco Research Institute of Chinese Academy of Agricultural Sciences)

  • Yanzhe Yang

    (Tobacco Research Institute of Chinese Academy of Agricultural Sciences)

  • Han Zhang

    (Tobacco Research Institute of Chinese Academy of Agricultural Sciences)

  • Chen Meng

    (Tobacco Research Institute of Chinese Academy of Agricultural Sciences)

  • Zhihong Xie

    (College of Resources and Environment of Shandong Agricultural University)

  • Xiaona Sui

    (Tobacco Research Institute of Chinese Academy of Agricultural Sciences)

  • Kangwen Xu

    (Tobacco Research Institute of Chinese Academy of Agricultural Sciences)

  • Yiqiang Li

    (Tobacco Research Institute of Chinese Academy of Agricultural Sciences)

  • Cheng-Sheng Zhang

    (Tobacco Research Institute of Chinese Academy of Agricultural Sciences)

Abstract

The root-associated microbiota plays an important role in the response to environmental stress. However, the underlying mechanisms controlling the interaction between salt-stressed plants and microbiota are poorly understood. Here, by focusing on a salt-tolerant plant wild soybean (Glycine soja), we demonstrate that highly conserved microbes dominated by Pseudomonas are enriched in the root and rhizosphere microbiota of salt-stressed plant. Two corresponding Pseudomonas isolates are confirmed to enhance the salt tolerance of wild soybean. Shotgun metagenomic and metatranscriptomic sequencing reveal that motility-associated genes, mainly chemotaxis and flagellar assembly, are significantly enriched and expressed in salt-treated samples. We further find that roots of salt stressed plants secreted purines, especially xanthine, which induce motility of the Pseudomonas isolates. Moreover, exogenous application for xanthine to non-stressed plants results in Pseudomonas enrichment, reproducing the microbiota shift in salt-stressed root. Finally, Pseudomonas mutant analysis shows that the motility related gene cheW is required for chemotaxis toward xanthine and for enhancing plant salt tolerance. Our study proposes that wild soybean recruits beneficial Pseudomonas species by exudating key metabolites (i.e., purine) against salt stress.

Suggested Citation

  • Yanfen Zheng & Xuwen Cao & Yanan Zhou & Siqi Ma & Youqiang Wang & Zhe Li & Donglin Zhao & Yanzhe Yang & Han Zhang & Chen Meng & Zhihong Xie & Xiaona Sui & Kangwen Xu & Yiqiang Li & Cheng-Sheng Zhang, 2024. "Purines enrich root-associated Pseudomonas and improve wild soybean growth under salt stress," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47773-9
    DOI: 10.1038/s41467-024-47773-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-47773-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-47773-9?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. Ling Xu & Zhaobin Dong & Dawn Chiniquy & Grady Pierroz & Siwen Deng & Cheng Gao & Spencer Diamond & Tuesday Simmons & Heidi M.-L. Wipf & Daniel Caddell & Nelle Varoquaux & Mary A. Madera & Robert Hutm, 2021. "Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    2. 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.
    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. 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.
    2. 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.
    3. 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.
    4. Luigi Russi & Gianpiero Marconi & Nicoletta Ferradini & Beatrice Farda & Marika Pellegrini & Loretta Pace, 2022. "Investigating Population Genetic Diversity and Rhizosphere Microbiota of Central Apennines’ Artemisia eriantha," Sustainability, MDPI, vol. 14(18), pages 1-14, September.
    5. Amrita Gupta & Udai B. Singh & Pramod K. Sahu & Surinder Paul & Adarsh Kumar & Deepti Malviya & Shailendra Singh & Pandiyan Kuppusamy & Prakash Singh & Diby Paul & Jai P. Rai & Harsh V. Singh & Madhab, 2022. "Linking Soil Microbial Diversity to Modern Agriculture Practices: A Review," IJERPH, MDPI, vol. 19(5), pages 1-29, March.
    6. 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.
    7. Sara M. Amolegbe & Adeline R. Lopez & Maria L. Velasco & Danielle J. Carlin & Michelle L. Heacock & Heather F. Henry & Brittany A. Trottier & William A. Suk, 2022. "Adapting to Climate Change: Leveraging Systems-Focused Multidisciplinary Research to Promote Resilience," IJERPH, MDPI, vol. 19(22), pages 1-18, November.
    8. 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.
    9. Ben O. Oyserman & Stalin Sarango Flores & Thom Griffioen & Xinya Pan & Elmar Wijk & Lotte Pronk & Wouter Lokhorst & Azkia Nurfikari & Joseph N. Paulson & Mercedeh Movassagh & Nejc Stopnisek & Anne Kup, 2022. "Disentangling the genetic basis of rhizosphere microbiome assembly in tomato," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    10. Adina Howe & Nejc Stopnisek & Shane K. Dooley & Fan Yang & Keara L. Grady & Ashley Shade, 2023. "Seasonal activities of the phyllosphere microbiome of perennial crops," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    11. Yunpeng Liu & Huihui Zhang & Jing Wang & Wenting Gao & Xiting Sun & Qin Xiong & Xia Shu & Youzhi Miao & Qirong Shen & Weibing Xun & Ruifu Zhang, 2024. "Nonpathogenic Pseudomonas syringae derivatives and its metabolites trigger the plant “cry for help” response to assemble disease suppressing and growth promoting rhizomicrobiome," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    12. Carla L. Abán & Giovanni Larama & Antonella Ducci & Jorgelina Huidobro & Michel Abanto & Silvina Vargas-Gil & Carolina Pérez-Brandan, 2022. "Soil Properties and Bacterial Communities Associated with the Rhizosphere of the Common Bean after Using Brachiaria brizantha as a Service Crop: A 10-Year Field Experiment," Sustainability, MDPI, vol. 15(1), pages 1-23, December.
    13. Ziwei Tao & Jinjuan Li & Hui Li & Guozhen Du, 2024. "Effects of High-Density Mixed Planting in Artificial Grassland on Microbial Community," Sustainability, MDPI, vol. 16(21), pages 1-16, October.
    14. 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.
    15. Wenli Zhang & Yubing Liu & Zengru Wang & Lina Zhao & Jinghua Qi & Yansong Wang & Pan Zhao & Naiqin Zhong, 2020. "Short-Term Effects of Eco-Friendly Fertilizers on a Soil Bacterial Community in the Topsoil and Rhizosphere of an Irrigated Agroecosystem," Sustainability, MDPI, vol. 12(12), pages 1-16, June.
    16. Nicholas Ozede Igiehon & Olubukola Oluranti Babalola, 2018. "Rhizosphere Microbiome Modulators: Contributions of Nitrogen Fixing Bacteria towards Sustainable Agriculture," IJERPH, MDPI, vol. 15(4), pages 1-25, March.

    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_s41467-024-47773-9. 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.