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The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus

Author

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  • Lene H. Madsen

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University)

  • Leïla Tirichine

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University
    †Present address: Génomique, Environnementale et Evolutive Section 3 CNRS UMR8197, Institut de Biologie de l'Ecole Normale Supérieure (IBENS), 46 rue d'Ulm, 75230 Paris Cedex 05, France)

  • Anna Jurkiewicz

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University)

  • John T. Sullivan

    (University of Otago, PO Box 56)

  • Anne B. Heckmann

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University)

  • Anita S. Bek

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University)

  • Clive W. Ronson

    (University of Otago, PO Box 56)

  • Euan K. James

    (Scottish Crop Research Institute, Invergowrie)

  • Jens Stougaard

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University)

Abstract

Bacterial infection of interior tissues of legume root nodules is controlled at the epidermal cell layer and is closely coordinated with progressing organ development. Using spontaneous nodulating Lotus japonicus plant mutants to uncouple nodule organogenesis from infection, we have determined the role of 16 genes in these two developmental processes. We show that host-encoded mechanisms control three alternative entry processes operating in the epidermis, the root cortex and at the single cell level. Single cell infection did not involve the formation of trans-cellular infection threads and was independent of host Nod-factor receptors and bacterial Nod-factor signals. In contrast, Nod-factor perception was required for epidermal root hair infection threads, whereas primary signal transduction genes preceding the secondary Ca2+ oscillations have an indirect role. We provide support for the origin of rhizobial infection through direct intercellular epidermal invasion and subsequent evolution of crack entry and root hair invasions observed in most extant legumes.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:1:y:2010:i:1:d:10.1038_ncomms1009
    DOI: 10.1038/ncomms1009
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    Cited by:

    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.

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