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.
Highlights
The establishment of fungal symbioses has been widely considered one of the key innovations that facilitated plant terrestrialization 460–480 million yr ago (Ma), since this was first hypothesised by Pirozynski & Malloch (1975)
Arbusculelike structures and vesicles characterize fungi fossilized within early Devonian vascular land plants (Stubblefield et al, 1987; Remy et al, 1994; Taylor et al, 1995), lending weight to the hypothesis that Glomeromycota fungi played a pivotal role in the evolution of land plants (Pirozynski & Malloch, 1975; Malloch et al, 1980; Selosse & Le Tacon, 1998)
Bryophytes are the most basal extant land plants and fungi associating with some extant thalloid liverworts have been identified as members of the Glomeromycota (Ligrone et al, 2007; Humphreys et al, 2010; Field et al, 2012)
Summary
The establishment of fungal symbioses has been widely considered one of the key innovations that facilitated plant terrestrialization 460–480 million yr ago (Ma), since this was first hypothesised by Pirozynski & Malloch (1975). Glomeromycota fungi were the only symbionts known to occur within basal land plant clades (the liverwort, hornwort and pteridophyte grades) on the basis of their characteristic intracellular arbuscules, vesicles and coils and largely aseptate hyphae (Ligrone, 1988; Selosse & Le Tacon, 1998; Read et al, 2000; Ligrone et al, 2007; Smith & Read, 2008). Bryophytes are the most basal extant land plants ( the exact order of divergence within the bryophytes remains under debate; see Cox et al, 2014) and fungi associating with some extant thalloid liverworts have been identified as members of the Glomeromycota (Ligrone et al, 2007; Humphreys et al, 2010; Field et al, 2012)
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