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Differential regulation of the Epr3 receptor coordinates membrane-restricted rhizobial colonization of root nodule primordia

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  • Yasuyuki Kawaharada

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University
    Present address: Department of Plant Bio Sciences, Faculty of Agriculture, Iwate University, 3-18-8 Ueda, Morioka, Iwate, Japan)

  • Mette W. Nielsen

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University)

  • Simon Kelly

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University)

  • Euan K. James

    (The James Hutton Institute, Invergowrie)

  • Kasper R. Andersen

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University)

  • Sheena R. Rasmussen

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University)

  • Winnie Füchtbauer

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University)

  • Lene H. Madsen

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University)

  • Anne B. Heckmann

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University
    Present address: Arla Foods Ingredients, Sønderhøj 10, 8260 Viby J, Denmark)

  • Simona Radutoiu

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University)

  • Jens Stougaard

    (Centre for Carbohydrate Recognition and Signalling, Aarhus University)

Abstract

In Lotus japonicus, a LysM receptor kinase, EPR3, distinguishes compatible and incompatible rhizobial exopolysaccharides at the epidermis. However, the role of this recognition system in bacterial colonization of the root interior is unknown. Here we show that EPR3 advances the intracellular infection mechanism that mediates infection thread invasion of the root cortex and nodule primordia. At the cellular level, Epr3 expression delineates progression of infection threads into nodule primordia and cortical infection thread formation is impaired in epr3 mutants. Genetic dissection of this developmental coordination showed that Epr3 is integrated into the symbiosis signal transduction pathways. Further analysis showed differential expression of Epr3 in the epidermis and cortical primordia and identified key transcription factors controlling this tissue specificity. These results suggest that exopolysaccharide recognition is reiterated during the progressing infection and that EPR3 perception of compatible exopolysaccharide promotes an intracellular cortical infection mechanism maintaining bacteria enclosed in plant membranes.

Suggested Citation

  • Yasuyuki Kawaharada & Mette W. Nielsen & Simon Kelly & Euan K. James & Kasper R. Andersen & Sheena R. Rasmussen & Winnie Füchtbauer & Lene H. Madsen & Anne B. Heckmann & Simona Radutoiu & Jens Stougaa, 2017. "Differential regulation of the Epr3 receptor coordinates membrane-restricted rhizobial colonization of root nodule primordia," Nature Communications, Nature, vol. 8(1), pages 1-11, April.
  • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_ncomms14534
    DOI: 10.1038/ncomms14534
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    Cited by:

    1. 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.
    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.

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