Journal
NEW PHYTOLOGIST
Volume 205, Issue 2, Pages 743-756Publisher
WILEY
DOI: 10.1111/nph.13024
Keywords
carbon dioxide; Endogone; Haplomitriopsida; Haplomitrium gibbsiae; liverwort; Mucoromycotina; mycorrhiza; Treubia lacunosa
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Funding
- NERC [NE/1024089/1]
- Leverhulme Emeritus Fellowship
- New Phytologist Trust
- NERC [NE/I024089/1, NE/I025360/1, NE/I027193/1] Funding Source: UKRI
- Natural Environment Research Council [NE/I024089/1, NE/I025360/1, NE/I027193/1] Funding Source: researchfish
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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 (1500ppm) and near-contemporary (440ppm) 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.
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