title: First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO2.
abstract: The discovery that Mucoromycotina, an ancient and partially saprotrophic fungal lineage, associates with the basal liverwort lineage Haplomitriopsida casts doubt on the widely held view that Glomeromycota formed the sole ancestral plant-fungus symbiosis. Whether this association is mutualistic, and how its functioning was affected by the fall in atmospheric CO2 concentration that followed plant terrestrialization in the Palaeozoic, remains unknown. We measured carbon-for-nutrient exchanges between Haplomitriopsida liverworts and Mucoromycotina fungi under simulated mid-Palaeozoic (1500 ppm) and near-contemporary (440 ppm) CO2 concentrations using isotope tracers, and analysed cytological differences in plant-fungal interactions. Concomitantly, we cultured both partners axenically, resynthesized the associations in vitro, and characterized their cytology. We demonstrate that liverwort-Mucoromycotina symbiosis is mutualistic and mycorrhiza-like, but differs from liverwort-Glomeromycota symbiosis in maintaining functional efficiency of carbon-for-nutrient exchange between partners across CO2 concentrations. Inoculation of axenic plants with Mucoromycotina caused major cytological changes affecting the anatomy of plant tissues, similar to that observed in wild-collected plants colonized by Mucoromycotina fungi. By demonstrating reciprocal exchange of carbon for nutrients between partners, our results provide support for Mucoromycotina establishing the earliest mutualistic symbiosis with land plants. As symbiotic functional efficiency was not compromised by reduced CO2 , we suggest that other factors led to the modern predominance of the Glomeromycota symbiosis.
authors.affiliation: Department of Animal and Plant Sciences, Western Bank, University of Sheffield, Sheffield, S10 2TN, UK.
authors.forename: Katie J
authors.initials: KJ
authors.lastname: Field
authors.forename: William R
authors.initials: WR
authors.lastname: Rimington
authors.forename: Martin I
authors.initials: MI
authors.lastname: Bidartondo
authors.forename: Kate E
authors.initials: KE
authors.lastname: Allinson
authors.forename: David J
authors.initials: DJ
authors.lastname: Beerling
authors.forename: Duncan D
authors.initials: DD
authors.lastname: Cameron
authors.forename: Jeffrey G
authors.initials: JG
authors.lastname: Duckett
authors.forename: Jonathan R
authors.initials: JR
authors.lastname: Leake
authors.forename: Silvia
authors.initials: S
authors.lastname: Pressel
mesh_terms: D001272:Atmosphere; D002244:Carbon / Q000378:metabolism; D002245:Carbon Dioxide; D019669:Embryophyta; D005658:Fungi / Q000166:cytology / Q000235:genetics / Q000502:physiology*; D035926:Hepatophyta / Q000502:physiology* / Q000648:ultrastructure; D008969:Molecular Sequence Data; D009584:Nitrogen / Q000378:metabolism; D010758:Phosphorus / Q000378:metabolism; D013559:Symbiosis / Q000502:physiology*
chemical_list: D002245:Carbon Dioxide; D010758:Phosphorus; D002244:Carbon; D009584:Nitrogen
keywords: Endogone; Haplomitriopsida; Haplomitrium gibbsiae; Mucoromycotina; Treubia lacunosa; carbon dioxide; liverwort; mycorrhiza