Origin and co-evolution of land plant-fungal symbioses through the "greening of the Earth"

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Colonization of the land by terrestrial plants ca. 475 Ma was one of themost far-reaching chapters in Earth's history. Liverworts occupy thepivotal position in the land plant evolutionary tree with a wide variety ofevidence supporting these non-vascular plants as the most basal terrestrialphotosynthetic organisms and amongst the earliest colonizers of the land ca.475 Ma. Recent molecular genetic evidence supports the view thatmycorrhiza-like associations in liverworts are a basal and ancestral trait,and land plants evolved from a single common ancestor that formed symbioticassociations with fungal partners before roots evolved. For at least the past 30 years, the prevailing paradigm has been that AMfungi are the ancestral form of all plant-fungal symbioses co-evolving withthe earliest land plants. AM associations are the most common type ofmycorrhiza, and are currently found in over 70% of land plant speciesincluding simple and complex thalloid liverworts. However, new evidencereported by members of the project team (MB, JGD, SP) has revealed that themost basal extant groups of liverworts, the Haplomitriopsida, exclusivelyform associations with the most basal group of plant-symbiotic fungi - theEndogonales. For the first time, we now have evidence pointing to theidentity of the fungal group at the dawn of their nutritional symbiosis withland plants. This opens a remarkable new window for functionalinvestigations into how the symbiosis facilitated the emergence of theterrestrial biosphere. Our proposal exploits these findings by addressing three fundamentalevolutionary questions relating to the initial phase of plants 'greening ofthe Earth':(1) Are the associations between liverworts and species of Endogonefunctionally equivalent to those formed with AM fungal partners? (2) Was the switching of fungal partners from facultatively saprotrophicEndogone to obligately biotrophic AM fungi through the evolutionary advanceof basal liverworts driven by increasing mutualistic benefits to the plantsand fungi?(3) Did the accumulation of soil organic matter favour obligately biotrophicAM fungi over facultatively saprotrophic Endogone in supplying mineralnutrients to the plants?We have carefully selected 7 liverwort species with fungal associations thatprovide a powerful spectrum of model systems amenable to experimentation andquantitative functional analyses of C exchange, nutrient relationships andfungal specificity. All of our target organisms can all be cultured eitherfrom spores or gemmae to provide plants with and without fungal symbionts.This provides a robust approach for enabling quantification of fungalcolonization on gametophyte growth, nutrition and reproductive output withina 3 yr project.Our experimental programme will be conducted on (1) mature field-collectedpopulations (and (2) symbiotic vs. asymbiotic plants grown fromgemmae/spores. Field collected populations will be used for functionalstudies of C-allocation from liverworts to their fungal partners andreciprocal uptake of nutrients into the plants via the fungi. Populationsfrom gemmae/spores will be used for investigating the net costs/benefits ofthe fungal symbionts on the growth and reproductive output of the liverwortsand the biomass and extent of the fungal partners. Molecular identificationand ultra-structural studies will be undertaken on both sets of plants toestablish the identity of the fungal endosymbionts, the nature of theplant-fungal interfaces, and how these relate to function and hostspecificity.Overall, this project will contribute fundamental knowledge andunderstanding to the dawn of an ancient symbiosis between land plants andfungi that played a founding role in the evolution of terrestrial ecosystems- a topic closely aligned to NERC's Earth System Science Theme high-levelchallenge "improving current knowledge of the interaction b