IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33908-3.html
   My bibliography  Save this article

Nutrient regulation of lipochitooligosaccharide recognition in plants via NSP1 and NSP2

Author

Listed:
  • Xin-Ran Li

    (University of Cambridge)

  • Jongho Sun

    (University of Cambridge)

  • Doris Albinsky

    (University of Cambridge)

  • Darius Zarrabian

    (University of Cambridge)

  • Raphaella Hull

    (University of Cambridge)

  • Tak Lee

    (University of Cambridge
    University of Cambridge)

  • Edwin Jarratt-Barnham

    (University of Cambridge)

  • Chai Hao Chiu

    (University of Cambridge)

  • Amy Jacobsen

    (University of Cambridge)

  • Eleni Soumpourou

    (University of Cambridge)

  • Alessio Albanese

    (University of Cambridge)

  • Wouter Kohlen

    (Wageningen University & Research)

  • Leonie H. Luginbuehl

    (John Innes Centre)

  • Bruno Guillotin

    (Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS
    NYU-Center of Genomic and System Biology)

  • Tom Lawrensen

    (John Innes Centre)

  • Hui Lin

    (John Innes Centre)

  • Jeremy Murray

    (John Innes Centre)

  • Emma Wallington

    (NIAB, 93 Lawrence Weaver Road)

  • Wendy Harwood

    (John Innes Centre)

  • Jeongmin Choi

    (University of Cambridge)

  • Uta Paszkowski

    (University of Cambridge)

  • Giles E. D. Oldroyd

    (University of Cambridge
    University of Cambridge)

Abstract

Many plants associate with arbuscular mycorrhizal fungi for nutrient acquisition, while legumes also associate with nitrogen-fixing rhizobial bacteria. Both associations rely on symbiosis signaling and here we show that cereals can perceive lipochitooligosaccharides (LCOs) for activation of symbiosis signaling, surprisingly including Nod factors produced by nitrogen-fixing bacteria. However, legumes show stringent perception of specifically decorated LCOs, that is absent in cereals. LCO perception in plants is activated by nutrient starvation, through transcriptional regulation of Nodulation Signaling Pathway (NSP)1 and NSP2. These transcription factors induce expression of an LCO receptor and act through the control of strigolactone biosynthesis and the karrikin-like receptor DWARF14-LIKE. We conclude that LCO production and perception is coordinately regulated by nutrient starvation to promote engagement with mycorrhizal fungi. Our work has implications for the use of both mycorrhizal and rhizobial associations for sustainable productivity in cereals.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33908-3
    DOI: 10.1038/s41467-022-33908-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33908-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-33908-3?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. Leïla Tirichine & Haruko Imaizumi-Anraku & Satoko Yoshida & Yasuhiro Murakami & Lene H. Madsen & Hiroki Miwa & Tomomi Nakagawa & Niels Sandal & Anita S. Albrektsen & Masayoshi Kawaguchi & Allan Downie, 2006. "Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development," Nature, Nature, vol. 441(7097), pages 1153-1156, June.
    2. Cynthia Gleason & Shubho Chaudhuri & Tianbao Yang & Alfonso Muñoz & B. W. Poovaiah & Giles E. D. Oldroyd, 2006. "Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition," Nature, Nature, vol. 441(7097), pages 1149-1152, June.
    3. J. Kruskal, 1964. "Nonmetric multidimensional scaling: A numerical method," Psychometrika, Springer;The Psychometric Society, vol. 29(2), pages 115-129, June.
    4. Ronelle Roth & Marco Chiapello & Héctor Montero & Peter Gehrig & Jonas Grossmann & Kevin O’Holleran & Denise Hartken & Fergus Walters & Shu-Yi Yang & Stefan Hillmer & Karin Schumacher & Sarah Bowden &, 2018. "A rice Serine/Threonine receptor-like kinase regulates arbuscular mycorrhizal symbiosis at the peri-arbuscular membrane," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    5. Hanqin Tian & Rongting Xu & Josep G. Canadell & Rona L. Thompson & Wilfried Winiwarter & Parvadha Suntharalingam & Eric A. Davidson & Philippe Ciais & Robert B. Jackson & Greet Janssens-Maenhout & Mic, 2020. "A comprehensive quantification of global nitrous oxide sources and sinks," Nature, Nature, vol. 586(7828), pages 248-256, October.
    6. Haruko Imaizumi-Anraku & Naoya Takeda & Myriam Charpentier & Jillian Perry & Hiroki Miwa & Yosuke Umehara & Hiroshi Kouchi & Yasuhiro Murakami & Lonneke Mulder & Kate Vickers & Jodie Pike & J. Allan D, 2005. "Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots," Nature, Nature, vol. 433(7025), pages 527-531, February.
    7. Jeongmin Choi & Tak Lee & Jungnam Cho & Emily K. Servante & Boas Pucker & William Summers & Sarah Bowden & Mehran Rahimi & Kyungsook An & Gynheung An & Harro J. Bouwmeester & Emma J. Wallington & Gile, 2020. "The negative regulator SMAX1 controls mycorrhizal symbiosis and strigolactone biosynthesis in rice," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    8. Gabriel Castrillo & Paulo José Pereira Lima Teixeira & Sur Herrera Paredes & Theresa F. Law & Laura de Lorenzo & Meghan E. Feltcher & Omri M. Finkel & Natalie W. Breakfield & Piotr Mieczkowski & Corbi, 2017. "Root microbiota drive direct integration of phosphate stress and immunity," Nature, Nature, vol. 543(7646), pages 513-518, March.
    9. 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.
    10. Julia Bailey-Serres & Jane E. Parker & Elizabeth A. Ainsworth & Giles E. D. Oldroyd & Julian I. Schroeder, 2019. "Genetic strategies for improving crop yields," Nature, Nature, vol. 575(7781), pages 109-118, November.
    11. Fabienne Maillet & Véréna Poinsot & Olivier André & Virginie Puech-Pagès & Alexandra Haouy & Monique Gueunier & Laurence Cromer & Delphine Giraudet & Damien Formey & Andreas Niebel & Eduardo Andres Ma, 2011. "Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza," Nature, Nature, vol. 469(7328), pages 58-63, January.
    12. Debatosh Das & Michael Paries & Karen Hobecker & Michael Gigl & Corinna Dawid & Hon-Ming Lam & Jianhua Zhang & Moxian Chen & Caroline Gutjahr, 2022. "PHOSPHATE STARVATION RESPONSE transcription factors enable arbuscular mycorrhiza symbiosis," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    13. Feng Feng & Jongho Sun & Guru V. Radhakrishnan & Tak Lee & Zoltán Bozsóki & Sébastien Fort & Aleksander Gavrin & Kira Gysel & Mikkel B. Thygesen & Kasper Røjkjær Andersen & Simona Radutoiu & Jens Stou, 2019. "A combination of chitooligosaccharide and lipochitooligosaccharide recognition promotes arbuscular mycorrhizal associations in Medicago truncatula," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    14. Tomás Allen Rush & Virginie Puech-Pagès & Adeline Bascaules & Patricia Jargeat & Fabienne Maillet & Alexandra Haouy & Arthur QuyManh Maës & Cristobal Carrera Carriel & Devanshi Khokhani & Michelle Kel, 2020. "Lipo-chitooligosaccharides as regulatory signals of fungal growth and development," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    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. Qiang Zhang & Shuangshuang Wang & Qiujin Xie & Yuanjun Xia & Lei Lu & Mingxing Wang & Gang Wang & Siyu Long & Yunfei Cai & Ling Xu & Ertao Wang & Yina Jiang, 2023. "Control of arbuscule development by a transcriptional negative feedback loop in Medicago," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Penelope L. Lindsay & Sergey Ivanov & Nathan Pumplin & Xinchun Zhang & Maria J. Harrison, 2022. "Distinct ankyrin repeat subdomains control VAPYRIN locations and intracellular accommodation functions during arbuscular mycorrhizal symbiosis," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. Ya Li & Hanqin Tian & Yuanzhi Yao & Hao Shi & Zihao Bian & Yu Shi & Siyuan Wang & Taylor Maavara & Ronny Lauerwald & Shufen Pan, 2024. "Increased nitrous oxide emissions from global lakes and reservoirs since the pre-industrial era," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    4. Beniaich, Adnane & Guimarães, Danielle Vieira & Avanzi, Junior Cesar & Silva, Bruno Montoani & Acuña-Guzman, Salvador Francisco & dos Santos, Wharley Pereira & Silva, Marx Leandro Naves, 2023. "Spontaneous vegetation as an alternative to cover crops in olive orchards reduces water erosion and improves soil physical properties under tropical conditions," Agricultural Water Management, Elsevier, vol. 279(C).
    5. Giuseppe Arbia & Giovanni Lafratta, 2002. "Anisotropic spatial sampling designs for urban pollution," Journal of the Royal Statistical Society Series C, Royal Statistical Society, vol. 51(2), pages 223-234, May.
    6. Aryal, Jeetendra P., 2022. "Contribution of Agriculture to Climate Change and Low-Emission Agricultural Development in Asia and the Pacific," ADBI Working Papers 1340, Asian Development Bank Institute.
    7. Samuel Shye, 2010. "The Motivation to Volunteer: A Systemic Quality of Life Theory," Social Indicators Research: An International and Interdisciplinary Journal for Quality-of-Life Measurement, Springer, vol. 98(2), pages 183-200, September.
    8. Kehinde Abraham Odelade & Olubukola Oluranti Babalola, 2019. "Bacteria, Fungi and Archaea Domains in Rhizospheric Soil and Their Effects in Enhancing Agricultural Productivity," IJERPH, MDPI, vol. 16(20), pages 1-19, October.
    9. Muñoz-Mas, Rafael & Vezza, Paolo & Alcaraz-Hernández, Juan Diego & Martínez-Capel, Francisco, 2016. "Risk of invasion predicted with support vector machines: A case study on northern pike (Esox Lucius, L.) and bleak (Alburnus alburnus, L.)," Ecological Modelling, Elsevier, vol. 342(C), pages 123-134.
    10. Cuihong Song & Jun-Jie Zhu & John L. Willis & Daniel P. Moore & Mark A. Zondlo & Zhiyong Jason Ren, 2024. "Oversimplification and misestimation of nitrous oxide emissions from wastewater treatment plants," Nature Sustainability, Nature, vol. 7(10), pages 1348-1358, October.
    11. Mengjie Qiao & Ruibo Sun & Zixuan Wang & Kenneth Dumack & Xingguang Xie & Chuanchao Dai & Ertao Wang & Jizhong Zhou & Bo Sun & Xinhua Peng & Michael Bonkowski & Yan Chen, 2024. "Legume rhizodeposition promotes nitrogen fixation by soil microbiota under crop diversification," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    12. la Grange, Anthony & le Roux, Niël & Gardner-Lubbe, Sugnet, 2009. "BiplotGUI: Interactive Biplots in R," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 30(i12).
    13. 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.
    14. Simensen, Trond & Halvorsen, Rune & Erikstad, Lars, 2018. "Methods for landscape characterisation and mapping: A systematic review," Land Use Policy, Elsevier, vol. 75(C), pages 557-569.
    15. Silvia Vilčeková & Ilija Zoran Apostoloski & Ľudmila Mečiarová & Eva Krídlová Burdová & Jozef Kiseľák, 2017. "Investigation of Indoor Air Quality in Houses of Macedonia," IJERPH, MDPI, vol. 14(1), pages 1-12, January.
    16. Shikai La & Jiafan Li & Si Ma & Xingqun Liu & Lihong Gao & Yongqiang Tian, 2024. "Protective role of native root-associated bacterial consortium against root-knot nematode infection in susceptible plants," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    17. Wu, Lihong & Quan, Hao & Wu, Lina & Zhang, Xi & Feng, Hao & Ding, Dianyuan & Siddique, Kadambot H.M., 2023. "Responses of winter wheat yield and water productivity to sowing time and plastic mulching in the Loess Plateau," Agricultural Water Management, Elsevier, vol. 289(C).
    18. Yukari Nagatoshi & Kenta Ikazaki & Yasufumi Kobayashi & Nobuyuki Mizuno & Ryohei Sugita & Yumiko Takebayashi & Mikiko Kojima & Hitoshi Sakakibara & Natsuko I. Kobayashi & Keitaro Tanoi & Kenichiro Fuj, 2023. "Phosphate starvation response precedes abscisic acid response under progressive mild drought in plants," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    19. 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.
    20. Funk, Patrick & Davis, Alex & Vaishnav, Parth & Dewitt, Barry & Fuchs, Erica, 2020. "Individual inconsistency and aggregate rationality: Overcoming inconsistencies in expert judgment at the technical frontier," Technological Forecasting and Social Change, Elsevier, vol. 155(C).

    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_s41467-022-33908-3. 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.