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Annexin- and calcium-regulated priming of legume root cells for endosymbiotic infection

Author

Listed:
  • Ambre Guillory

    (LIPME, INRAE, CNRS, Université de Toulouse)

  • Joëlle Fournier

    (LIPME, INRAE, CNRS, Université de Toulouse)

  • Audrey Kelner

    (LIPME, INRAE, CNRS, Université de Toulouse)

  • Karen Hobecker

    (Max-Planck-Institute of Molecular Plant Physiology)

  • Marie-Christine Auriac

    (LIPME, INRAE, CNRS, Université de Toulouse)

  • Lisa Frances

    (LIPME, INRAE, CNRS, Université de Toulouse)

  • Anaïs Delers

    (LIPME, INRAE, CNRS, Université de Toulouse)

  • Léa Pedinotti

    (LRSV, Université de Toulouse, CNRS, UPS, Toulouse INP)

  • Aurélie Ru

    (Université de Toulouse, CNRS, UPS)

  • Jean Keller

    (LRSV, Université de Toulouse, CNRS, UPS, Toulouse INP)

  • Pierre-Marc Delaux

    (LRSV, Université de Toulouse, CNRS, UPS, Toulouse INP)

  • Caroline Gutjahr

    (Max-Planck-Institute of Molecular Plant Physiology)

  • Nicolas Frei Dit Frey

    (LRSV, Université de Toulouse, CNRS, UPS, Toulouse INP)

  • Fernanda Carvalho-Niebel

    (LIPME, INRAE, CNRS, Université de Toulouse)

Abstract

Legumes establish endosymbioses with arbuscular mycorrhizal (AM) fungi or rhizobia bacteria to improve mineral nutrition. Symbionts are hosted in privileged habitats, root cortex (for AM fungi) or nodules (for rhizobia) for efficient nutrient exchange. To reach these habitats, plants form cytoplasmic cell bridges, key to predicting and guiding fungal hyphae or rhizobia-filled infection thread (IT) root entry. However, the underlying mechanisms are poorly studied. Here we show that unique ultrastructural changes and calcium (Ca2+) spiking signatures, closely associated with Medicago truncatula Annexin 1 (MtAnn1) accumulation, accompany rhizobia-related bridge formation. Loss of MtAnn1 function in M. truncatula affects Ca2+ spike amplitude, cytoplasmic configuration and rhizobia infection efficiency, consistent with a role of MtAnn1 in regulating infection priming. MtAnn1, which evolved in species establishing intracellular symbioses, is also AM-symbiosis-induced and required for proper arbuscule formation. Together, we propose that MtAnn1 is part of an ancient Ca2+-regulatory module for transcellular endosymbiotic infection.

Suggested Citation

  • Ambre Guillory & Joëlle Fournier & Audrey Kelner & Karen Hobecker & Marie-Christine Auriac & Lisa Frances & Anaïs Delers & Léa Pedinotti & Aurélie Ru & Jean Keller & Pierre-Marc Delaux & Caroline Gutj, 2024. "Annexin- and calcium-regulated priming of legume root cells for endosymbiotic infection," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-55067-3
    DOI: 10.1038/s41467-024-55067-3
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    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. Cheng-Wu Liu & Andrew Breakspear & Nicola Stacey & Kim Findlay & Jin Nakashima & Karunakaran Ramakrishnan & Miaoxia Liu & Fang Xie & Gabriella Endre & Fernanda Carvalho-Niebel & Giles E. D. Oldroyd & , 2019. "A protein complex required for polar growth of rhizobial infection threads," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
    3. Robert C. Edgar, 2022. "Muscle5: High-accuracy alignment ensembles enable unbiased assessments of sequence homology and phylogeny," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    4. Volker Gerke & Felicity N. E. Gavins & Michael Geisow & Thomas Grewal & Jyoti K. Jaiswal & Jesper Nylandsted & Ursula Rescher, 2024. "Annexins—a family of proteins with distinctive tastes for cell signaling and membrane dynamics," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
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