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The B-type response regulator GmRR11d mediates systemic inhibition of symbiotic nodulation

Author

Listed:
  • Jiahuan Chen

    (Huazhong Agricultural University)

  • Zhijuan Wang

    (Huazhong Agricultural University)

  • Lixiang Wang

    (Huazhong Agricultural University
    Shanxi Agricultural University)

  • Yangyang Hu

    (Huazhong Agricultural University)

  • Qiqi Yan

    (Huazhong Agricultural University)

  • Jingjing Lu

    (Huazhong Agricultural University)

  • Ziyin Ren

    (Huazhong Agricultural University)

  • Yujie Hong

    (Huazhong Agricultural University)

  • Hongtao Ji

    (Huazhong Agricultural University)

  • Hui Wang

    (Huazhong Agricultural University)

  • Xinying Wu

    (Huazhong Agricultural University)

  • Yanru Lin

    (Huazhong Agricultural University)

  • Chao Su

    (Faculty of Biology, Cell Biology)

  • Thomas Ott

    (Faculty of Biology, Cell Biology
    University of Freiburg)

  • Xia Li

    (Huazhong Agricultural University
    Guangdong Laboratory for Lingnan Modern Agriculture, Wushan Road, Guangzhou)

Abstract

Key to the success of legumes is the ability to form and maintain optimal symbiotic nodules that enable them to balance the trade-off between symbiosis and plant growth. Cytokinin is essential for homeostatic regulation of nodulation, but the mechanism remains incompletely understood. Here, we show that a B-type response regulator GmRR11d mediates systemic inhibition of nodulation. GmRR11d is induced by rhizobia and low level cytokinin, and GmRR11d can suppress the transcriptional activity of GmNSP1 on GmNIN1a to inhibit soybean nodulation. GmRR11d positively regulates cytokinin response and its binding on the GmNIN1a promoter is enhanced by cytokinin. Intriguingly, rhizobial induction of GmRR11d and its function are dependent upon GmNARK that is a CLV1-like receptor kinase and inhibits nodule number in shoots. Thus, GmRR11d governs a transcriptional program associated with nodulation attenuation and cytokinin response activation essential for systemic regulation of nodulation.

Suggested Citation

  • Jiahuan Chen & Zhijuan Wang & Lixiang Wang & Yangyang Hu & Qiqi Yan & Jingjing Lu & Ziyin Ren & Yujie Hong & Hongtao Ji & Hui Wang & Xinying Wu & Yanru Lin & Chao Su & Thomas Ott & Xia Li, 2022. "The B-type response regulator GmRR11d mediates systemic inhibition of symbiotic nodulation," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35360-9
    DOI: 10.1038/s41467-022-35360-9
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    References listed on IDEAS

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    1. Takashi Kurakawa & Nanae Ueda & Masahiko Maekawa & Kaoru Kobayashi & Mikiko Kojima & Yasuo Nagato & Hitoshi Sakakibara & Junko Kyozuka, 2007. "Direct control of shoot meristem activity by a cytokinin-activating enzyme," Nature, Nature, vol. 445(7128), pages 652-655, February.
    2. Simona Radutoiu & Lene Heegaard Madsen & Esben Bjørn Madsen & Hubert H. Felle & Yosuke Umehara & Mette Grønlund & Shusei Sato & Yasukazu Nakamura & Satoshi Tabata & Niels Sandal & Jens Stougaard, 2003. "Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases," Nature, Nature, vol. 425(6958), pages 585-592, October.
    3. Carole Laffont & Ariel Ivanovici & Pierre Gautrat & Mathias Brault & Michael Anthony Djordjevic & Florian Frugier, 2020. "The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    4. Lene Krusell & Lene H. Madsen & Shusei Sato & Grégoire Aubert & Aratz Genua & Krzysztof Szczyglowski & Gérard Duc & Takakazu Kaneko & Satoshi Tabata & Frans de Bruijn & Eloisa Pajuelo & Niels Sandal &, 2002. "Shoot control of root development and nodulation is mediated by a receptor-like kinase," Nature, Nature, vol. 420(6914), pages 422-426, November.
    5. Satoru Okamoto & Hidefumi Shinohara & Tomoko Mori & Yoshikatsu Matsubayashi & Masayoshi Kawaguchi, 2013. "Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase," Nature Communications, Nature, vol. 4(1), pages 1-7, October.
    6. Esben Bjørn Madsen & Lene Heegaard Madsen & Simona Radutoiu & Magdalena Olbryt & Magdalena Rakwalska & Krzysztof Szczyglowski & Shusei Sato & Takakazu Kaneko & Satoshi Tabata & Niels Sandal & Jens Sto, 2003. "A receptor kinase gene of the LysM type is involved in legumeperception of rhizobial signals," Nature, Nature, vol. 425(6958), pages 637-640, October.
    7. Rieko Nishimura & Masaki Hayashi & Guo-Jiang Wu & Hiroshi Kouchi & Haruko Imaizumi-Anraku & Yasuhiro Murakami & Shinji Kawasaki & Shoichiro Akao & Masayuki Ohmori & Mamoru Nagasawa & Kyuya Harada & Ma, 2002. "HAR1 mediates systemic regulation of symbiotic organ development," Nature, Nature, vol. 420(6914), pages 426-429, November.
    8. Mingtang Xie & Hongyu Chen & Ling Huang & Ryan C. O’Neil & Maxim N. Shokhirev & Joseph R. Ecker, 2018. "A B-ARR-mediated cytokinin transcriptional network directs hormone cross-regulation and shoot development," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    9. Takema Sasaki & Takuya Suzaki & Takashi Soyano & Mikiko Kojima & Hitoshi Sakakibara & Masayoshi Kawaguchi, 2014. "Shoot-derived cytokinins systemically regulate root nodulation," Nature Communications, Nature, vol. 5(1), pages 1-9, December.
    10. 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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