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

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 g...

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Autores principales: Brottier, Laurent, Chaintreuil, Clémence, Simion, Paul, Scornavacca, Céline, Rivallan, Ronan, Mournet, Pierre, Moulin, Lionel, Lewis, Gwilym P., Fardoux, Joël, Brown, Spencer C., Gomez-Pacheco, Mario, Bourges, Mickaël, Hervouet, Catherine, Gueye, Mathieu, Duponnois, Robin, Ramanankierana, Heriniaina, Randriambanona, Herizo, Vandrot, Hervé, Zabaleta, Maria, DasGupta, Maitrayee, D’Hont, Angélique, Giraud, Eric, Arrighi, Jean-François
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6282307/
https://www.ncbi.nlm.nih.gov/pubmed/30518342
http://dx.doi.org/10.1186/s12870-018-1567-z
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author Brottier, Laurent
Chaintreuil, Clémence
Simion, Paul
Scornavacca, Céline
Rivallan, Ronan
Mournet, Pierre
Moulin, Lionel
Lewis, Gwilym P.
Fardoux, Joël
Brown, Spencer C.
Gomez-Pacheco, Mario
Bourges, Mickaël
Hervouet, Catherine
Gueye, Mathieu
Duponnois, Robin
Ramanankierana, Heriniaina
Randriambanona, Herizo
Vandrot, Hervé
Zabaleta, Maria
DasGupta, Maitrayee
D’Hont, Angélique
Giraud, Eric
Arrighi, Jean-François
author_facet Brottier, Laurent
Chaintreuil, Clémence
Simion, Paul
Scornavacca, Céline
Rivallan, Ronan
Mournet, Pierre
Moulin, Lionel
Lewis, Gwilym P.
Fardoux, Joël
Brown, Spencer C.
Gomez-Pacheco, Mario
Bourges, Mickaël
Hervouet, Catherine
Gueye, Mathieu
Duponnois, Robin
Ramanankierana, Heriniaina
Randriambanona, Herizo
Vandrot, Hervé
Zabaleta, Maria
DasGupta, Maitrayee
D’Hont, Angélique
Giraud, Eric
Arrighi, Jean-François
author_sort Brottier, Laurent
collection PubMed
description 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1567-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-62823072018-12-10 A phylogenetic framework of the legume genus Aeschynomene for comparative genetic analysis of the Nod-dependent and Nod-independent symbioses Brottier, Laurent Chaintreuil, Clémence Simion, Paul Scornavacca, Céline Rivallan, Ronan Mournet, Pierre Moulin, Lionel Lewis, Gwilym P. Fardoux, Joël Brown, Spencer C. Gomez-Pacheco, Mario Bourges, Mickaël Hervouet, Catherine Gueye, Mathieu Duponnois, Robin Ramanankierana, Heriniaina Randriambanona, Herizo Vandrot, Hervé Zabaleta, Maria DasGupta, Maitrayee D’Hont, Angélique Giraud, Eric Arrighi, Jean-François BMC Plant Biol Research Article 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1567-z) contains supplementary material, which is available to authorized users. BioMed Central 2018-12-05 /pmc/articles/PMC6282307/ /pubmed/30518342 http://dx.doi.org/10.1186/s12870-018-1567-z Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Brottier, Laurent
Chaintreuil, Clémence
Simion, Paul
Scornavacca, Céline
Rivallan, Ronan
Mournet, Pierre
Moulin, Lionel
Lewis, Gwilym P.
Fardoux, Joël
Brown, Spencer C.
Gomez-Pacheco, Mario
Bourges, Mickaël
Hervouet, Catherine
Gueye, Mathieu
Duponnois, Robin
Ramanankierana, Heriniaina
Randriambanona, Herizo
Vandrot, Hervé
Zabaleta, Maria
DasGupta, Maitrayee
D’Hont, Angélique
Giraud, Eric
Arrighi, Jean-François
A phylogenetic framework of the legume genus Aeschynomene for comparative genetic analysis of the Nod-dependent and Nod-independent symbioses
title A phylogenetic framework of the legume genus Aeschynomene for comparative genetic analysis of the Nod-dependent and Nod-independent symbioses
title_full A phylogenetic framework of the legume genus Aeschynomene for comparative genetic analysis of the Nod-dependent and Nod-independent symbioses
title_fullStr A phylogenetic framework of the legume genus Aeschynomene for comparative genetic analysis of the Nod-dependent and Nod-independent symbioses
title_full_unstemmed A phylogenetic framework of the legume genus Aeschynomene for comparative genetic analysis of the Nod-dependent and Nod-independent symbioses
title_short A phylogenetic framework of the legume genus Aeschynomene for comparative genetic analysis of the Nod-dependent and Nod-independent symbioses
title_sort phylogenetic framework of the legume genus aeschynomene for comparative genetic analysis of the nod-dependent and nod-independent symbioses
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6282307/
https://www.ncbi.nlm.nih.gov/pubmed/30518342
http://dx.doi.org/10.1186/s12870-018-1567-z
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