The ecology and evolution of fungal symbiosis in ancient land plants

Abstract

Mycorrhizas are the mutualistic symbioses shared between fungi and the vast majority of land plants. These relationships provide present day plants with many nutritional and functional benefits and were key to the movement of plants onto land over 500 million years ago. This thesis concerns the mycorrhizal-like symbioses of early- diverging liverworts, some of the closest living relatives of the first land plants. The study of arbuscular mycorrhizal fungi, Glomeromycotina, in 674 globally collected liverworts has provided molecular evidence to support that the formation of arbuscular mycorrhizas, the most common type of mycorrhizal symbiosis, is an ancestral trait of all land plants. The early-diverging Glomeromycotina families were found to be ten times more common in liverworts than flowering plants. Mucoromycotina fungi potentially formed the first fungal symbiosis with plants. Mucoromycotina symbiosis, like Glomeromycotina, was regularly found throughout the early-diverging liverworts, many of which can be simultaneously colonised by both fungal lineages. Mucoromycotina and Glomeromycotina symbioses were found to differ in their origins, lifestyles and network characteristics. Through the use of cophylogeny analyses it was discovered that liverworts and their fungal symbionts have coevolved. The symbiotic relationships shared between Treubia liverworts and Mucoromycotina fungi appear to be more coevolved than those shared between Marchantia liverworts and Glomeromycotina. The fungal symbiosis status of over 590 species of liverworts, hornworts and lycopods has been compiled by combining the data produced here with previous publications. While symbioses are very common in hornworts and lycopods, it is estimated that less than 30% of liverwort species enter into these relationships. These investigations have uncovered the diversity and distribution of Mucoromycotina and Glomeromycotina symbioses in liverworts. Discovering that these relationships are fundamentally different impacts our understanding of the ecology and evolution of fungal symbioses in land plants and has implications in their future potential use in sustainable agriculture.