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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
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    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. 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.
    4. 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.
    5. 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.
    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.
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