Evolution of DMSP (dimethylsulfoniopropionate) biosynthesis pathway: Origin and phylogenetic distribution in polyploid Spartina (Poaceae, Chloridoideae)

Hélène Rousseau (1) , Mathieu Rousseau-Gueutin (2) , Xavier Dauvergne (3) , Julien Boutte (1) , Gaëlle Simon (4) , Nathalie Marnet (5) , Alain Bouchereau (2) , Solene Guiheneuf (6) , Jean-Pierre Bazureau (6) , Jérôme Morice (2) , Stephane Ravanel (7) , Francisco Cabello-Hurtado (1) , Abdelkader Aïnouche (1) , Armel Salmon (1) , Jonathan F. Wendel (8) , Malika L. Ainouche (1)

1 ECOBIO - Ecosystèmes, biodiversité, évolution [Rennes]
2 IGEPP - Institut de Génétique, Environnement et Protection des Plantes
3 Institut de Géoarchitecture
4 RMN-RPE-SM - Plateforme technologique de Résonance Magnétique Nucléaire et de Résonance Paramagnétique Electronique
5 INRA - Institut National de la Recherche Agronomique
6 ISCR - Institut des Sciences Chimiques de Rennes
7 LPCV - Physiologie cellulaire et végétale
8 ISU - Iowa State University

DMSP (dimethylsulfoniopropionate) is an ecologically important sulfur metabolite commonly produced by marine algae and by some higher plant lineages, including the polyploid salt marsh genus Spartina (Poaceae). The molecular mechanisms and genes involved in the DMSP biosynthesis pathways are still unknown. In this study, we performed comparative analyses of DMSP amounts and molecular phylogenetic analyses to decipher the origin of DMSP in Spartina that represents one of the major source of terrestrial DMSP in coastal marshes. DMSP content was explored in 14 Spartina species using (1)H Nuclear Magnetic Resonance (NMR) spectroscopy and Ultra Performance Liquid Chromatography-Mass Spectrometry (UPLC-MS). Putative genes encoding the four enzymatic steps of the DMSP biosynthesis pathway in Spartina were examined and their evolutionary dynamics were studied. We found that the hexaploid lineage containing S. alterniflora, S. foliosa and S. maritima and their derived hybrids and allopolyploids are all able to produce DMSP, in contrast to species in the tetraploid clade. Thus, examination of DMSP synthesis in a phylogenetic context implicated a single origin of this physiological innovation, which occurred in the ancestor of the hexaploid Spartina lineage, 3-6MYA. Candidate genes specific to the Spartina DMSP biosynthesis pathway were also retrieved from Spartina transcriptomes, and provide a framework for future investigations to decipher the molecular mechanisms involved in this plant phenotypic novelty that has major ecological impacts in saltmarsh ecosystems.

Keywords: genome duplication; Gene phylogeny; Cordgrass; Phenotypic novelty

Domains: Environmental Sciences; Biodiversity and Ecology

Hélène Rousseau, Mathieu Rousseau-Gueutin, Xavier Dauvergne, Julien Boutte, Gaëlle Simon, et al.. Evolution of DMSP (dimethylsulfoniopropionate) biosynthesis pathway: Origin and phylogenetic distribution in polyploid Spartina (Poaceae, Chloridoideae). Molecular Phylogenetics and Evolution, 2017, 114, pp.401-414. ⟨10.1016/j.ympev.2017.07.003⟩. ⟨hal-01579439⟩