IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-35360-9.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-35360-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-35360-9?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. 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. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
    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. Jieshun Lin & Yuda Purwana Roswanjaya & Wouter Kohlen & Jens Stougaard & Dugald Reid, 2021. "Nitrate restricts nodule organogenesis through inhibition of cytokinin biosynthesis in Lotus japonicus," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. Manuel Frank & Lavinia Ioana Fechete & Francesca Tedeschi & Marcin Nadzieja & Malita Malou Malekzadeh Nørgaard & Jesus Montiel & Kasper Røjkjær Andersen & Mikkel H. Schierup & Dugald Reid & Stig Ugger, 2023. "Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicus," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    3. Giuseppe Malgioglio & Giulio Flavio Rizzo & Sebastian Nigro & Vincent Lefebvre du Prey & Joelle Herforth-Rahmé & Vittoria Catara & Ferdinando Branca, 2022. "Plant-Microbe Interaction in Sustainable Agriculture: The Factors That May Influence the Efficacy of PGPM Application," Sustainability, MDPI, vol. 14(4), pages 1-28, February.
    4. Ning Zhou & Xiaolin Li & Zhiqiong Zheng & Jing Liu & J. Allan Downie & Fang Xie, 2024. "RinRK1 enhances NF receptors accumulation in nanodomain-like structures at root-hair tip," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. Ke Tao & Ib T. Jensen & Sha Zhang & Eber Villa-Rodríguez & Zuzana Blahovska & Camilla Lind Salomonsen & Anna Martyn & Þuríður Nótt Björgvinsdóttir & Simon Kelly & Luc Janss & Marianne Glasius & Rasmus, 2024. "Nitrogen and Nod factor signaling determine Lotus japonicus root exudate composition and bacterial assembly," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    6. Anna Kokla & Martina Leso & Xiang Zhang & Jan Simura & Phanu T. Serivichyaswat & Songkui Cui & Karin Ljung & Satoko Yoshida & Charles W. Melnyk, 2022. "Nitrogen represses haustoria formation through abscisic acid in the parasitic plant Phtheirospermum japonicum," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    7. Keyi Ye & Fengjiao Bu & Liyuan Zhong & Zhaonian Dong & Zhaoxu Ma & Zhanpeng Tang & Yu Zhang & Xueyong Yang & Xun Xu & Ertao Wang & William J. Lucas & Sanwen Huang & Huan Liu & Jianshu Zheng, 2024. "Mapping the molecular landscape of Lotus japonicus nodule organogenesis through spatiotemporal transcriptomics," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    8. Pierre Gautrat & Sara Buti & Andrés Romanowski & Michiel Lammers & Sanne E. A. Matton & Guido Buijs & Ronald Pierik, 2024. "Phytochrome-dependent responsiveness to root-derived cytokinins enables coordinated elongation responses to combined light and nitrate cues," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. 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.
    10. Sanfeng Li & Yuchun Rao & Penggen Duan & Zhonghao Wang & Ping Hu & Ruoqian Yu & Chenxi Luo & Mengna Tang & Caolin Lu & Yuexing Wang & Yijian Mao, 2023. "Mapping and Candidate Gene Prediction of qPL7-25 : A Panicle Length QTL in Dongxiang Wild Rice," Agriculture, MDPI, vol. 13(8), pages 1-15, August.
    11. Moritz Sexauer & Hemal Bhasin & Maria Schön & Elena Roitsch & Caroline Wall & Ulrike Herzog & Katharina Markmann, 2023. "A micro RNA mediates shoot control of root branching," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    12. Le Yu & Wenting Zhou & Yixuan She & Hongmin Ma & You-Sheng Cai & Ming Jiang & Zixin Deng & Neil P. J. Price & Wenqing Chen, 2021. "Efficient biosynthesis of nucleoside cytokinin angustmycin A containing an unusual sugar system," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    13. Wilfried Chevalier & Sitti-Anlati Moussa & Miguel Medeiros Netto Ottoni & Cécile Dubois-Laurent & Sébastien Huet & Christophe Aubert & Elsa Desnoues & Brigitte Navez & Valentine Cottet & Guillaume Cha, 2021. "Multisite evaluation of phenotypic plasticity for specialized metabolites, some involved in carrot quality and disease resistance," PLOS ONE, Public Library of Science, vol. 16(4), pages 1-22, April.

    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:13:y:2022:i:1:d:10.1038_s41467-022-35360-9. 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.