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

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, Duanmu De-Qiang (), Yue-Feng Guan () and Zhi-Chang Chen ()
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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
Duanmu De-Qiang: Huazhong Agricultural University
Yue-Feng Guan: Guangzhou University
Zhi-Chang Chen: Fujian Agriculture and Forestry University

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-53325-y

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