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.

Special relationship between fungi and plants may have spurred changes to ancient climate

“…-Christine Strullu-Derrien than they did at low, modern carbon dioxide levels-in contrast to Field's results with gloms (4,9). So why would ancient plants partner with mucs that were less efficient in that atmosphere, especially if gloms were an option?…”

“…Field headed to New Zealand to collect some of the muc-liverwort partners. Her chamber experiments showed they did indeed make the exchange (9).…”

Evolutionary signals of symbiotic persistence in the legume–rhizobia mutualism

“…Rather, it illustrates the types of questions and variables that can be addressed. Other factors, such as historic atmospheric CO 2 concentrations (98), have been thought to affect the evolution and stability of other plant root mutualisms (99,100) and could likewise be considered in this framework.…”

On plant defense signaling networks and early land plant evolution

“…Several bryophytes form mycorrhizae by interacting with fungi [24,27,28], but the picture for bryophytes as a whole is patchy [29]. While many liverworts (outlined above) and hornworts [30,31] exhibit interactions with mycorrhizal fungi, mosses generally do not form mycorrhizae [32,33]; for a recent and comprehensive overview see [29].…”