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

Abstract

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 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.

Gene and Transposable Element Expression Evolution Following Recent and Past Polyploidy Events in Spartina (Poaceae)

“…Polyploidy and hybridization have important adaptive consequences in Spartina. Hexaploid species evolved anatomical and physiological traits [including salt and xenobiotic tolerance increased by specific cells such as salt glands or trichomes, production of DMSP (Dimethylsulfoniopropionate), an osmoprotectant molecule; Céccoli et al, 2015;Paredes-Páliz et al, 2017;Robertson et al, 2017;Rousseau et al, 2017;Cavé-Radet et al, 2019b] providing the ability to colonize low marsh zones and tolerate several hours of tidal immersion (Maricle et al, 2009;Bedre et al, 2016). Invasive abilities appear as an immediate consequence of hybridization and/or genome duplication in Spartina (Strong and Ayres, 2013;Ainouche and Gray, 2016).…”

In Vitro Reconstitution of Bacterial DMSP Biosynthesis

“…Only the methionine S‐methyltransferase MSMT (route 2 and 3), and the methylthiohydroxybutryate S‐methyltransferase DsyB (route 1), have been identified and directly linked to DMSP production. Complete sets of DMSP biosynthetic enzymes are unknown . In this report, the full in vitro reconstitution of DMSP biosynthesis from Streptomyces mobaraensis is described.…”

Mechanistic insight into DsyB/DSYB, key enzymes in marine dimethylsulfoniopropionate synthesis

“…Three pathways for DMSP synthesis have been proposed based on the identi cation of intermediates and enzyme activities in various model DMSP producers: a methylation pathway in some plants and bacteria, a transamination pathway in algae and bacteria, and a decarboxylation pathway in one dino agellate (10,(12)(13)(14)(15) (Fig. 1).…”