SHIFTING SYMBIOTIC SCENARIOS AT THE DAWN OF LAND PLANT-FUNGUS ASSOCIATIONS

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Plants colonised Earth's landmasses more than 475 Ma, drastically altering the development of the terrestrial biosphere, with far-reaching consequences for all subsequent terrestrial life. It is widely thought that symbiotic fungi facilitated early plant terrestrialisation by enhancing access to mineral nutrients in exchange for photosynthetically-fixed organic carbon. Our recent discoveries have brought into question the hitherto-assumed identity, biology and function of the fungal symbionts of the earliest diverging lineages of extant land plants. Our project addresses these fundamental knowledge gaps, including critical new questions arising from our previous research about the regulation and compatibility of plant-fungal associations. This project promises fascinating discoveries into the intertwined past, present and future of plants, microbes and soils.More than 80% of plants today associate with soil-dwelling fungi called Glomeromycota, forming mutually beneficial partnerships known as arbuscular mycorrhizas (AM). These cooperative partnerships involve the transfer of plant sugars, produced through photosynthesis, to fungal partners in return for essential nutrients mined from minerals in the soil by the fungi. When the first rootless plants emerged from water onto dry land more the 475 million years ago, it is thought that cooperative fungi provided the nutrients that plants needed to grow on land. Recent research by members of the project team has shown that some of the most evolutionarily ancient plants on Earth, the liverworts, form partnerships with fungi that are probably more evolutionarily ancient than AM. These fungi are called Mucoromycotina. Our findings suggest that associations between liverworts and Mucoromycotina fungi may be ancestral to the mycorrhizal symbiosis, paving the way for the colonisation of the terrestrial environment by plants and the evolution of the intricate terrestrial ecosystems that we are familiar with today. It is equally possible that the earliest land plants actually associated with both Mucoromycotina and AM simultaneously, as some plants still do today. For more than 30 years there has been a focus on AM as the ancestral plant-fungal symbiosis but with our surprising recent discovery of an alternative globally widespread and ancient association, we have the unique opportunity and pressing need to understand a new biology with potentially myriad ramifications for life on Earth.By using cutting-edge and novel methodologies from different fields of science, our research will generate crucial insights into the functioning and compatibility of cooperation between both groups of fungi with several major groups of land plants. Our experiments will be carried out under different atmospheric CO2 concentrations, reflecting the changing CO2 concentrations on Earth through evolutionary time, providing exciting new insights into the structure, function and evolution of modern plant-fungal symbioses.Through a deeper mechanistic and evolutionary understanding of the interaction between CO2 and diverse soil fungi, our research expands into wider aspects of soil ecology, plant-soil processes, and may lead to more efficient conservation strategies (see Pathways to Impact document). Through examining the physiological responses of symbiosis through different groups of land plants, this research will aid understanding and prediction of responses of these systems to ongoing changes in atmospheric CO2 concentrations; important considerations within the NERC Climate System and Biodiversity strategies, and with major implications for food security and soil ecology. Looking further into the future, the techniques and hypotheses that we develop and test through this research are transferable to other economically-important symbioses within the plant kingdom, such as fungal diseases of crops and the use of mycorrhizas in crops for future sustainable agriculture.