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A phylogenetic framework of the legume genus Aeschynomene for comparative genetic analysis of the Nod-dependent and Nod-independent symbioses

Laurent Brottier 1 Clémence Chaintreuil 1, 2 Paul Simion 3 Celine Scornavacca 3 Ronan Rivallan 4 Pierre Mournet 4 Lionel Moulin 1 Gwilym Lewis 5 Joël Fardoux 1, 2 Spencer Brown 6 Mario Gomez-Pacheco 7 Mickaël Bourges 7 Catherine Hervouet 8 Mathieu Gueye 9 Robin Duponnois 1, 2 Heriniaina Ramanankierana 10 Herizo Randriambanona 11 Hervé Vandrot 12, 13 Maria Zabaleta 14 Maitrayee Dasgupta 14 Angélique D’hont 4 Eric Giraud 1, 2 Jean-François Arrighi 1, 2
1 UMR LSTM - Laboratoire des symbioses tropicales et méditerranéennes
2 IRD - Institut de Recherche pour le Développement
3 UMR ISEM - Institut des Sciences de l'Evolution de Montpellier
4 UMR AGAP - Amélioration génétique et adaptation des plantes méditerranéennes et tropicales
5 Royal Botanic Gardens Kew
6 ISV - Institut des sciences du végétal
7 I2BC - Institut de Biologie Intégrative de la Cellule
8 TIRO-MATOs - UMR E4320 - Transporteurs et Imagerie, Radiothérapie en Oncologie et Mécanismes biologiques des Altérations du Tissu Osseux
TIRO-MATOs - UMR E4320 : UMR E4320, SHFJ - Service Hospitalier Frédéric Joliot
9 IFAN - Institut Fondamental d'Afrique Noire - Laboratoire de botanique
10 Centre National de Recherches sur l'Environnement
11 CNRE - Centre National de Recherche sur l'Environnement
12 IAC - Institut Agronomique Néo-Calédonien
13 UMR AMAP - Botanique et Modélisation de l'Architecture des Plantes et des Végétations
14 IIBCE - Instituto de Investigaciones Biológicas Clemente Estable [Montevideo]
Abstract : Background: Among semi-aquatic species of the legume genus Aeschynomene, some have the property of being nodulated by photosynthetic Bradyrhizobium lacking the nodABC genes necessary for the synthesis of Nod factors. Knowledge of the specificities underlying this Nod-independent symbiosis has been gained from the model legume Aeschynomene evenia but our understanding remains limited due to the lack of comparative genetics with related taxa using a Nod factor-dependent process. To fill this gap, we combined different approaches to perform a thorough comparative analysis in the genus Aeschynomene. Results: This study significantly broadened previous taxon sampling, including in allied genera, in order to construct a comprehensive phylogeny. In the phylogenetic tree, five main lineages were delineated, including a novel lineage, the Nod-independent clade and another one containing a polytomy that comprised several Aeschynomene groups and all the allied genera. This phylogeny was matched with data on chromosome number, genome size and low-copy nuclear gene sequences to reveal the diploid species and a polytomy containing mostly polyploid taxa. For these taxa, a single allopolyploid origin was inferred and the putative parental lineages were identified. Finally, nodulation tests with different Bradyrhizobium strains revealed new nodulation behaviours and the diploid species outside of the Nod-independent clade were compared for their experimental tractability and genetic diversity. Conclusions: The extended knowledge of the genetics and biology of the different lineages sheds new light of the evolutionary history of the genus Aeschynomene and they provide a solid framework to exploit efficiently the diversity encountered in Aeschynomene legumes. Notably, our backbone tree contains all the species that are diploid and it clarifies the genetic relationships between the Nod-independent clade and the Nod-dependent lineages. This study enabled the identification of A. americana and A. patula as the most suitable species to undertake a comparative genetic study of the Nod-independent and Nod-dependent symbioses.
Keywords : Symbiosis Fabaceae Phylogenetics Polyploidy Nodulation Aeschynomene Genetics Legumes
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UNIV-MONTPELLIER | CNRS | INRA | CEA | AGROPOLIS | CEA-UPSAY | CIRAD | IRD | BA | UNICE | I2BC | UNIV-COTEDAZUR | CEA-DRF | B3ESTE | ISEM | AMAP | BIAM | CEA-CAD | JOLIOT | EPHE | MONTPELLIER-SUPAGRO | SHFJ | INRAE | PSL

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Laurent Brottier, Clémence Chaintreuil, Paul Simion, Celine Scornavacca, Ronan Rivallan, et al.. A phylogenetic framework of the legume genus Aeschynomene for comparative genetic analysis of the Nod-dependent and Nod-independent symbioses. BMC Plant Biology, BioMed Central, 2018, 18 (1), ⟨10.1186/s12870-018-1567-z⟩. ⟨hal-01961745⟩

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