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IMA peptides regulate root nodulation and nitrogen homeostasis by providing iron according to internal nitrogen status

Author

Listed:
  • Momoyo Ito

    (University of Tsukuba)

  • Yuri Tajima

    (University of Tsukuba
    Rhelixa Inc.)

  • Mari Ogawa-Ohnishi

    (Nagoya University)

  • Hanna Nishida

    (National Agriculture and Food Research Organization)

  • Shohei Nosaki

    (University of Tsukuba
    University of Tsukuba)

  • Momona Noda

    (University of Tsukuba)

  • Naoyuki Sotta

    (The University of Tokyo)

  • Kensuke Kawade

    (National Institute for Basic Biology
    The Graduate University for Advanced Studies (SOKENDAI)
    Saitama University)

  • Takehiro Kamiya

    (The University of Tokyo)

  • Toru Fujiwara

    (The University of Tokyo)

  • Yoshikatsu Matsubayashi

    (Nagoya University)

  • Takuya Suzaki

    (University of Tsukuba
    University of Tsukuba)

Abstract

Legumes control root nodule symbiosis (RNS) in response to environmental nitrogen availability. Despite the recent understanding of the molecular basis of external nitrate-mediated control of RNS, it remains mostly elusive how plants regulate physiological processes depending on internal nitrogen status. In addition, iron (Fe) acts as an essential element that enables symbiotic nitrogen fixation; however, the mechanism of Fe accumulation in nodules is poorly understood. Here, we focus on the transcriptome in response to internal nitrogen status during RNS in Lotus japonicus and identify that IRON MAN (IMA) peptide genes are expressed during symbiotic nitrogen fixation. We show that LjIMA1 and LjIMA2 expressed in the shoot and root play systemic and local roles in concentrating internal Fe to the nodule. Furthermore, IMA peptides have conserved roles in regulating nitrogen homeostasis by adjusting nitrogen-Fe balance in L. japonicus and Arabidopsis thaliana. These findings indicate that IMA-mediated Fe provision plays an essential role in regulating nitrogen-related physiological processes.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44865-4
    DOI: 10.1038/s41467-024-44865-4
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    References listed on IDEAS

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    1. Nao Okuma & Takashi Soyano & Takuya Suzaki & Masayoshi Kawaguchi, 2020. "MIR2111-5 locus and shoot-accumulated mature miR2111 systemically enhance nodulation depending on HAR1 in Lotus japonicus," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    2. Chloé Marchive & François Roudier & Loren Castaings & Virginie Bréhaut & Eddy Blondet & Vincent Colot & Christian Meyer & Anne Krapp, 2013. "Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants," Nature Communications, Nature, vol. 4(1), pages 1-9, June.
    3. Takanori Kobayashi & Seiji Nagasaka & Takeshi Senoura & Reiko Nakanishi Itai & Hiromi Nakanishi & Naoko K. Nishizawa, 2013. "Iron-binding haemerythrin RING ubiquitin ligases regulate plant iron responses and accumulation," Nature Communications, Nature, vol. 4(1), pages 1-12, December.
    4. Takushi Hachiya & Jun Inaba & Mayumi Wakazaki & Mayuko Sato & Kiminori Toyooka & Atsuko Miyagi & Maki Kawai-Yamada & Daisuke Sugiura & Tsuyoshi Nakagawa & Takatoshi Kiba & Alain Gojon & Hitoshi Sakaki, 2021. "Excessive ammonium assimilation by plastidic glutamine synthetase causes ammonium toxicity in Arabidopsis thaliana," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    5. Hanna Nishida & Sachiko Tanaka & Yoshihiro Handa & Momoyo Ito & Yuki Sakamoto & Sachihiro Matsunaga & Shigeyuki Betsuyaku & Kenji Miura & Takashi Soyano & Masayoshi Kawaguchi & Takuya Suzaki, 2018. "A NIN-LIKE PROTEIN mediates nitrate-induced control of root nodule symbiosis in Lotus japonicus," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    6. Leif Schauser & Andreas Roussis & Jiri Stiller & Jens Stougaard, 1999. "A plant regulator controlling development of symbiotic root nodules," Nature, Nature, vol. 402(6758), pages 191-195, November.
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    1. 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.

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