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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
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    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
    11. J. Kruskal, 1964. "Nonmetric multidimensional scaling: A numerical method," Psychometrika, Springer;The Psychometric Society, vol. 29(2), pages 115-129, June.
    12. 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.
    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.
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