IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-53325-y.html
   My bibliography  Save this article

Inorganic nitrogen inhibits symbiotic nitrogen fixation through blocking NRAMP2-mediated iron delivery in soybean nodules

Author

Listed:
  • Min Zhou

    (Fujian Agriculture and Forestry University)

  • Yuan Li

    (Fujian Agriculture and Forestry University)

  • Xiao-Lei Yao

    (Fujian Agriculture and Forestry University)

  • Jing Zhang

    (Fujian Agriculture and Forestry University)

  • Sheng Liu

    (Fujian Agriculture and Forestry University)

  • Hong-Rui Cao

    (Fujian Agriculture and Forestry University)

  • Shuang Bai

    (Fujian Agriculture and Forestry University)

  • Chun-Qu Chen

    (Fujian Agriculture and Forestry University)

  • Dan-Xun Zhang

    (Fujian Agriculture and Forestry University)

  • Ao Xu

    (Fujian Agriculture and Forestry University)

  • Jia-Ning Lei

    (Ningbo University)

  • Qian-Zhuo Mao

    (Ningbo University)

  • Yu Zhou

    (Huazhong Agricultural University)

  • De-Qiang Duanmu

    (Huazhong Agricultural University)

  • Yue-Feng Guan

    (Guangzhou University)

  • Zhi-Chang Chen

    (Fujian Agriculture and Forestry University)

Abstract

Symbiotic nitrogen fixation (SNF) in legume-rhizobia serves as a sustainable source of nitrogen (N) in agriculture. However, the addition of inorganic N fertilizers significantly inhibits SNF, and the underlying mechanisms remain not-well understood. Here, we report that inorganic N disrupts iron (Fe) homeostasis in soybean nodules, leading to a decrease in SNF efficiency. This disruption is attributed to the inhibition of the Fe transporter genes Natural Resistance-Associated Macrophage Protein 2a and 2b (GmNRAMP2a&2b) by inorganic N. GmNRAMP2a&2b are predominantly localized at the tonoplast of uninfected nodule tissues, affecting Fe transfer to infected cells and consequently, modulating SNF efficiency. In addition, we identified a pair of N-signal regulators, nitrogen-regulated GARP-type transcription factors 1a and 1b (GmNIGT1a&1b), that negatively regulate the expression of GmNRAMP2a&2b, which establishes a link between N signaling and Fe homeostasis in nodules. Our findings reveal a plausible mechanism by which soybean adjusts SNF efficiency through Fe allocation in response to fluctuating inorganic N conditions, offering valuable insights for optimizing N and Fe management in legume-based agricultural systems.

Suggested Citation

  • Min Zhou & Yuan Li & Xiao-Lei Yao & Jing Zhang & Sheng Liu & Hong-Rui Cao & Shuang Bai & Chun-Qu Chen & Dan-Xun Zhang & Ao Xu & Jia-Ning Lei & Qian-Zhuo Mao & Yu Zhou & De-Qiang Duanmu & Yue-Feng Guan, 2024. "Inorganic nitrogen inhibits symbiotic nitrogen fixation through blocking NRAMP2-mediated iron delivery in soybean nodules," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53325-y
    DOI: 10.1038/s41467-024-53325-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-53325-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-53325-y?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. Momoyo Ito & Yuri Tajima & Mari Ogawa-Ohnishi & Hanna Nishida & Shohei Nosaki & Momona Noda & Naoyuki Sotta & Kensuke Kawade & Takehiro Kamiya & Toru Fujiwara & Yoshikatsu Matsubayashi & Takuya Suzaki, 2024. "IMA peptides regulate root nodulation and nitrogen homeostasis by providing iron according to internal nitrogen status," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Mark A. Sutton & Oene Oenema & Jan Willem Erisman & Adrian Leip & Hans van Grinsven & Wilfried Winiwarter, 2011. "Too much of a good thing," Nature, Nature, vol. 472(7342), pages 159-161, April.
    3. Xin Wang & Zhimin Qiu & Wenjun Zhu & Nan Wang & Mengyan Bai & Huaqin Kuang & Chenlin Cai & Xiangbin Zhong & Fanjiang Kong & Peitao Lü & Yuefeng Guan, 2023. "The NAC transcription factors SNAP1/2/3/4 are central regulators mediating high nitrogen responses in mature nodules of soybean," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Mineko Konishi & Shuichi Yanagisawa, 2013. "Arabidopsis NIN-like transcription factors have a central role in nitrate signalling," Nature Communications, Nature, vol. 4(1), pages 1-9, June.
    5. Mohamed A. El-Brolosy & Zacharias Kontarakis & Andrea Rossi & Carsten Kuenne & Stefan Günther & Nana Fukuda & Khrievono Kikhi & Giulia L. M. Boezio & Carter M. Takacs & Shih-Lei Lai & Ryuichi Fukuda &, 2019. "Genetic compensation triggered by mutant mRNA degradation," Nature, Nature, vol. 568(7751), pages 193-197, April.
    6. Zhipeng Ma & Peipei Zhu & Hui Shi & Liwei Guo & Qinghe Zhang & Yanan Chen & Shuming Chen & Zhe Zhang & Jinrong Peng & Jun Chen, 2019. "PTC-bearing mRNA elicits a genetic compensation response via Upf3a and COMPASS components," Nature, Nature, vol. 568(7751), pages 259-263, April.
    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. Antonios Apostolopoulos & Naohiro Kawamoto & Siu Yu A. Chow & Hitomi Tsuiji & Yoshiho Ikeuchi & Yuichi Shichino & Shintaro Iwasaki, 2024. "dCas13-mediated translational repression for accurate gene silencing in mammalian cells," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Federica Diofano & Karolina Weinmann & Isabelle Schneider & Kevin D Thiessen & Wolfgang Rottbauer & Steffen Just, 2020. "Genetic compensation prevents myopathy and heart failure in an in vivo model of Bag3 deficiency," PLOS Genetics, Public Library of Science, vol. 16(11), pages 1-24, November.
    3. Juqi Zou & Satoshi Anai & Satoshi Ota & Shizuka Ishitani & Masayuki Oginuma & Tohru Ishitani, 2023. "Determining zebrafish dorsal organizer size by a negative feedback loop between canonical/non-canonical Wnts and Tlr4/NFκB," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Meyer-Aurich, Andreas & Karatay, Yusuf Nadi, 2019. "Effects of uncertainty and farmers' risk aversion on optimal N fertilizer supply in wheat production in Germany," Agricultural Systems, Elsevier, vol. 173(C), pages 130-139.
    5. Simon Anastasiadis & Marie-Laure Nauleau & Suzi Kerr & Tim Cox & Kit Rutherford, 2011. "Does Complex Hydrology Require Complex Water Quality Policy? NManager Simulations for Lake Rotorua," Working Papers 11_14, Motu Economic and Public Policy Research.
    6. Ledgard, Stewart F. & Wei, Sha & Wang, Xiaoqin & Falconer, Shelley & Zhang, Nannan & Zhang, Xiying & Ma, Lin, 2019. "Nitrogen and carbon footprints of dairy farm systems in China and New Zealand, as influenced by productivity, feed sources and mitigations," Agricultural Water Management, Elsevier, vol. 213(C), pages 155-163.
    7. Charné Viljoen & Janke van der Colf & Pieter Andreas Swanepoel, 2020. "Benefits Are Limited with High Nitrogen Fertiliser Rates in Kikuyu-Ryegrass Pasture Systems," Land, MDPI, vol. 9(6), pages 1-20, May.
    8. Cathal Buckley & Paul Murphy & David Wall, 2013. "Farm-gate N and P balances and use efficiencies across specialist dairy farms in the Republic Ireland," Working Papers 1302, Rural Economy and Development Programme,Teagasc.
    9. Andreas Meyer-Aurich & Jørgen Olesen & Annette Prochnow & Reiner Brunsch, 2013. "Greenhouse gas mitigation with scarce land: The potential contribution of increased nitrogen input," Mitigation and Adaptation Strategies for Global Change, Springer, vol. 18(7), pages 921-932, October.
    10. Yusuf Nadi Karatay & Andreas Meyer-Aurich, 2018. "A Model Approach for Yield-Zone-Specific Cost Estimation of Greenhouse Gas Mitigation by Nitrogen Fertilizer Reduction," Sustainability, MDPI, vol. 10(3), pages 1-18, March.
    11. Cecilia Bellora & Élodie Blanc & Jean-Marc Bourgeon & Eric Strobl, 2018. "Estimating the Impact of Crop Diversity on Agricultural Productivity in South Africa," NBER Chapters, in: Agricultural Productivity and Producer Behavior, pages 185-215, National Bureau of Economic Research, Inc.
    12. Sandra Lage & Zivan Gojkovic & Christiane Funk & Francesco G. Gentili, 2018. "Algal Biomass from Wastewater and Flue Gases as a Source of Bioenergy," Energies, MDPI, vol. 11(3), pages 1-30, March.
    13. Ahmmed Md Motasim & Abd Wahid Samsuri & Arina Shairah Abdul Sukor & Amin Mohd Adibah, 2021. "Gaseous Nitrogen Losses from Tropical Soils with Liquid or Granular Urea Fertilizer Application," Sustainability, MDPI, vol. 13(6), pages 1-11, March.
    14. Vishnu Muraleedharan Saraswathy & Lili Zhou & Mayssa H. Mokalled, 2024. "Single-cell analysis of innate spinal cord regeneration identifies intersecting modes of neuronal repair," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    15. Zehui Liu & Harald E. Rieder & Christian Schmidt & Monika Mayer & Yixin Guo & Wilfried Winiwarter & Lin Zhang, 2023. "Optimal reactive nitrogen control pathways identified for cost-effective PM2.5 mitigation in Europe," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    16. Thomas Juan & Agatha Ribeiro da Silva & Bárbara Cardoso & SoEun Lim & Violette Charteau & Didier Y. R. Stainier, 2023. "Multiple pkd and piezo gene family members are required for atrioventricular valve formation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    17. Castro Campos, Bente & Petrick, Martin, 2020. "Agricultural Land Use, Local Political Power, and Groundwater Nitrate Contamination in Germany," 60th Annual Conference, Halle/ Saale, Germany, September 23-25, 2020 305583, German Association of Agricultural Economists (GEWISOLA).
    18. Gong, Aolin & Mieno, Taro & Bullock, David S., 2022. "Using On-farm Precision Experimentation Data to Analyse Maximum Return to Nitrogen (MRTN) Recommendations," Agri-Tech Economics Papers 337140, Harper Adams University, Land, Farm & Agribusiness Management Department.
    19. Koesling, Matthias & Hansen, Sissel & Bleken, Marina Azzaroli, 2017. "Variations in nitrogen utilisation on conventional and organic dairy farms in Norway," Agricultural Systems, Elsevier, vol. 157(C), pages 11-21.
    20. Meijiang Gao & Marina Veil & Marcus Rosenblatt & Aileen Julia Riesle & Anna Gebhard & Helge Hass & Lenka Buryanova & Lev Y. Yampolsky & Björn Grüning & Sergey V. Ulianov & Jens Timmer & Daria Onichtch, 2022. "Pluripotency factors determine gene expression repertoire at zygotic genome activation," Nature Communications, Nature, vol. 13(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_s41467-024-53325-y. 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.