IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-26820-9.html
   My bibliography  Save this article

Nitrate restricts nodule organogenesis through inhibition of cytokinin biosynthesis in Lotus japonicus

Author

Listed:
  • Jieshun Lin

    (Aarhus University)

  • Yuda Purwana Roswanjaya

    (Wageningen University
    Agency for the Assessment and Application of Technology (BPPT))

  • Wouter Kohlen

    (Wageningen University)

  • Jens Stougaard

    (Aarhus University)

  • Dugald Reid

    (Aarhus University)

Abstract

Legumes balance nitrogen acquisition from soil nitrate with symbiotic nitrogen fixation. Nitrogen fixation requires establishment of a new organ, which is a cytokinin dependent developmental process in the root. We found cytokinin biosynthesis is a central integrator, balancing nitrate signalling with symbiotic acquired nitrogen. Low nitrate conditions provide a permissive state for induction of cytokinin by symbiotic signalling and thus nodule development. In contrast, high nitrate is inhibitory to cytokinin accumulation and nodule establishment in the root zone susceptible to nodule formation. This reduction of symbiotic cytokinin accumulation was further exacerbated in cytokinin biosynthesis mutants, which display hypersensitivity to nitrate inhibition of nodule development, maturation and nitrogen fixation. Consistent with this, cytokinin application rescues nodulation and nitrogen fixation of biosynthesis mutants in a concentration dependent manner. These inhibitory impacts of nitrate on symbiosis occur in a Nlp1 and Nlp4 dependent manner and contrast with the positive influence of nitrate on cytokinin biosynthesis that occurs in species that do not form symbiotic root nodules. Altogether this shows that legumes, as exemplified by Lotus japonicus, have evolved a different cytokinin response to nitrate compared to non-legumes.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26820-9
    DOI: 10.1038/s41467-021-26820-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-26820-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-021-26820-9?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. Kewei Zhang & Ondrej Novak & Zhaoyang Wei & Mingyue Gou & Xuebin Zhang & Yong Yu & Huijun Yang & Yuanheng Cai & Miroslav Strnad & Chang-Jun Liu, 2014. "Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins," Nature Communications, Nature, vol. 5(1), pages 1-12, May.
    2. Kun-hsiang Liu & Yajie Niu & Mineko Konishi & Yue Wu & Hao Du & Hoo Sun Chung & Lei Li & Marie Boudsocq & Matthew McCormack & Shugo Maekawa & Tetsuya Ishida & Chao Zhang & Kevan Shokat & Shuichi Yanag, 2017. "Discovery of nitrate–CPK–NLP signalling in central nutrient–growth networks," Nature, Nature, vol. 545(7654), pages 311-316, May.
    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. 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.
    5. Lene H. Madsen & Leïla Tirichine & Anna Jurkiewicz & John T. Sullivan & Anne B. Heckmann & Anita S. Bek & Clive W. Ronson & Euan K. James & Jens Stougaard, 2010. "The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus," Nature Communications, Nature, vol. 1(1), pages 1-12, December.
    6. Yoshie Maeda & Mineko Konishi & Takatoshi Kiba & Yasuhito Sakuraba & Naoya Sawaki & Tomohiro Kurai & Yoshiaki Ueda & Hitoshi Sakakibara & Shuichi Yanagisawa, 2018. "A NIGT1-centred transcriptional cascade regulates nitrate signalling and incorporates phosphorus starvation signals in Arabidopsis," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    7. 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.
    8. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. 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.
    2. 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.

    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. 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. 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.
    3. 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.
    4. 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.
    5. Pan Liao & Itay Maoz & Meng-Ling Shih & Ji Hee Lee & Xing-Qi Huang & John A. Morgan & Natalia Dudareva, 2023. "Emission of floral volatiles is facilitated by cell-wall non-specific lipid transfer proteins," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. 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.
    7. Kei Hiruma & Seishiro Aoki & Junya Takino & Takeshi Higa & Yuniar Devi Utami & Akito Shiina & Masanori Okamoto & Masami Nakamura & Nanami Kawamura & Yoshihiro Ohmori & Ryohei Sugita & Keitaro Tanoi & , 2023. "A fungal sesquiterpene biosynthesis gene cluster critical for mutualist-pathogen transition in Colletotrichum tofieldiae," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    8. 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.
    9. Sanghwa Lee & Julia Showalter & Ling Zhang & Gaëlle Cassin-Ross & Hatem Rouached & Wolfgang Busch, 2024. "Nutrient levels control root growth responses to high ambient temperature in plants," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    10. Yasuhito Sakuraba & Mailun Yang & Shuichi Yanagisawa, 2024. "HASTY-mediated miRNA dynamics modulate nitrogen starvation-induced leaf senescence in Arabidopsis," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    11. 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.
    12. 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.
    13. 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.
    14. Xin-Ran Li & Jongho Sun & Doris Albinsky & Darius Zarrabian & Raphaella Hull & Tak Lee & Edwin Jarratt-Barnham & Chai Hao Chiu & Amy Jacobsen & Eleni Soumpourou & Alessio Albanese & Wouter Kohlen & Le, 2022. "Nutrient regulation of lipochitooligosaccharide recognition in plants via NSP1 and NSP2," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    15. Kishan Mahmud & Dinesh Panday & Anaas Mergoum & Ali Missaoui, 2021. "Nitrogen Losses and Potential Mitigation Strategies for a Sustainable Agroecosystem," Sustainability, MDPI, vol. 13(4), pages 1-23, February.

    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:12:y:2021:i:1:d:10.1038_s41467-021-26820-9. 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.