Comparative phylotranscriptomics reveals a 110 million years-old symbiotic program

Autor: Cyril Libourel, Jean Keller, Lukas Brichet, Anne-Claire Cazalé, Sébastien Carrère, Tatiana Vernié, Jean-Malo Couzigou, Caroline Callot, Isabelle Dufau, Stéphane Cauet, William Marande, Tabatha Bulach, Amandine Suin, Catherine Masson-Boivin, Philippe Remigi, Pierre-Marc Delaux, Delphine Capela
Přispěvatelé: Laboratoire de Recherche en Sciences Végétales (LRSV), Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT), Laboratoire des Interactions Plantes Microbes Environnement (LIPME), Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Centre National de Ressources Génomiques Végétales (CNRGV), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Génome et Transcriptome - Plateforme Génomique ( GeT-PlaGe), Plateforme Génome & Transcriptome (GET), Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Université de Toulouse (UT)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), French National Research Institute for Agriculture, Food and Environment (INRAE, Plant Health and Environment Division), Fédération de Recherche Agrobiosciences, Interactions et Biodiversité, project Engineering Nitrogen Symbiosis for Africa (ENSA) currently funded through a grant to the University of Cambridge by the Bill & Melinda Gates Foundation (OPP1172165) and the UK Foreign, Commonwealth and Development Office as Engineering Nitrogen Symbiosis for Africa (OPP1172165)., European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement No 101001675 - ORIGINS), ANR-10-LABX-0041,TULIP,Towards a Unified theory of biotic Interactions: the roLe of environmental(2010), ANR-18-EURE-0019,TULIP-GSR,The Toulouse-Perpignan(2018), European Project: 609398,EC:FP7:PEOPLE,FP7-PEOPLE-2013-COFUND,AGREENSKILLSPLUS(2014)
Jazyk: angličtina
Rok vydání: 2022
Předmět:
Popis: SummarySymbiotic interactions have structured past and present ecosystems and shaped the evolution of life. As any trait, the symbiotic state observed in extant species builds on ancestral and conserved features, and lineage-specific innovations. From these mixed origins, defining the ancestral state of symbiotic associations is challenging although it is instrumental for understanding how symbiotic abilities emerge from non-symbiotic states. Here we aimed at reconstructing the intermediate steps leading to the root-nodule nitrogen-fixing symbiosis (RNS) observed in some extant flowering plants. For this, we compared the transcriptomic responses of nine host plants in response to symbiotic bacteria. We included the mimosoid legume Mimosa pudica for which we assembled a chromosome-level genome and generated the transcriptomic response to experimentally evolved bacterial symbionts. With this dataset, we reconstructed the ancestral RNS transcriptome, composed of most already described symbiotic genes together with hundreds of novel candidates. We found that the response to the chemical signals produced by the symbiont, nodule organogenesis and nitrogen-fixation are predominantly linked to ancestral responses, although these traits have diversified in the different nitrogen-fixing lineages. We detected a clear signature of recent and convergent evolution for the ability to release intracellular symbiosomes in two legume lineages, exemplified by the expression of different classes of small proteins in each group, potentially leading to the convergent gain of symbiotic evolutionary stability. Our findings demonstrate that most of the novelties for RNS were mostly in place in the most recent common ancestor of the RNS-forming species that lived on Earth 110 million years ago.Graphical abstractA little graphical/nice phylogeny with nodes of interestHighlightsWe sequenced a high-quality genome of the Mimosoideae Mimosa pudicaThe nitrogen-fixing root-nodule symbiosis relies on an ancestral transcriptomic responseAll symbiotic traits involve genes of the ancestral symbiotic programSymbiont perception, nodule organogenesis and nitrogen-fixation are essentially ancestral processesConvergent evolution of intracellular accommodation of symbionts additionally involves lineage-specific genes
Databáze: OpenAIRE