Genetics of nodulation in Aeschynomene evenia uncovers mechanisms of the rhizobium–legume symbiosis

Johan Quilbé, Léo Lamy, Laurent Brottier, Philippe Leleux, Joël Fardoux, Ronan Rivallan, Thomas Benichou, Rémi Guyonnet, Manuel Becana, Irene Villar, Olivier Garsmeur, Bárbara Hufnagel, Amandine Delteil, Djamel Gully, Clémence Chaintreuil, Marjorie Pervent, Fabienne Cartieaux, Mickaël Bourge, Nicolas Valentin, Guillaume Martin, Loïc Fontaine, Gaëtan Droc, Alexis Dereeper, Andrew Farmer, Cyril Libourel, Nico Nouwen, Frédéric Gressent, Pierre Mournet, Angélique D’Hont, Eric Giraud, Christophe Klopp and Jean-François Arrighi ()
Additional contact information
Johan Quilbé: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J
Léo Lamy: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J
Laurent Brottier: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J
Philippe Leleux: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J
Joël Fardoux: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J
Ronan Rivallan: CIRAD, UMR AGAP
Thomas Benichou: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J
Rémi Guyonnet: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J
Manuel Becana: Consejo Superior de Investigaciones Científicas
Irene Villar: Consejo Superior de Investigaciones Científicas
Olivier Garsmeur: CIRAD, UMR AGAP
Bárbara Hufnagel: BPMP, Université de Montpellier, CNRS, INRAE, SupAgro
Amandine Delteil: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J
Djamel Gully: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J
Clémence Chaintreuil: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J
Marjorie Pervent: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J
Fabienne Cartieaux: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J
Mickaël Bourge: Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC)
Nicolas Valentin: Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC)
Guillaume Martin: CIRAD, UMR AGAP
Loïc Fontaine: BGPI, Université de Montpellier, CIRAD, INRA, Montpellier SupAgro
Gaëtan Droc: CIRAD, UMR AGAP
Alexis Dereeper: University of Montpellier, DIADE, IPME
Andrew Farmer: National Center for Genome Resources
Cyril Libourel: LRSV, Université de Toulouse, CNRS, UPS
Nico Nouwen: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J
Frédéric Gressent: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J
Pierre Mournet: CIRAD, UMR AGAP
Angélique D’Hont: CIRAD, UMR AGAP
Eric Giraud: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J
Christophe Klopp: Genotoul, BioinfoMics, UR875 Biométrie et Intelligence Artificielle, INRAE
Jean-François Arrighi: IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), UMR IRD/ SupAgro/INRAE/ UM2 /CIRAD, TA-A82/J

Nature Communications, 2021, vol. 12, issue 1, 1-14

Abstract: Abstract Among legumes (Fabaceae) capable of nitrogen-fixing nodulation, several Aeschynomene spp. use a unique symbiotic process that is independent of Nod factors and infection threads. They are also distinctive in developing root and stem nodules with photosynthetic bradyrhizobia. Despite the significance of these symbiotic features, their understanding remains limited. To overcome such limitations, we conduct genetic studies of nodulation in Aeschynomene evenia, supported by the development of a genome sequence for A. evenia and transcriptomic resources for 10 additional Aeschynomene spp. Comparative analysis of symbiotic genes substantiates singular mechanisms in the early and late nodulation steps. A forward genetic screen also shows that AeCRK, coding a receptor-like kinase, and the symbiotic signaling genes AePOLLUX, AeCCamK, AeCYCLOPS, AeNSP2, and AeNIN are required to trigger both root and stem nodulation. This work demonstrates the utility of the A. evenia model and provides a cornerstone to unravel mechanisms underlying the rhizobium–legume symbiosis.

Date: 2021
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DOI: 10.1038/s41467-021-21094-7

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