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

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 Gutjahr, Nicolas Frei Dit Frey and Fernanda Carvalho-Niebel ()
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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

Nature Communications, 2024, vol. 15, issue 1, 1-21

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-55067-3

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