Functional analysis of liverworts in dual symbiosis with Glomeromycota and Mucoromycotina fungi under a simulated Palaeozoic CO2 decline

Abstract

Most land plants form mutualistic associations with arbuscular mycorrhizal fungi of the Glomeromycota, but recent studies have found that ancient plant lineages form mutualisms with Mucoromycotina fungi. Simultaneous associations with both fungal lineages have now been found in some plants, necessitating studies to understand the functional and evolutionary significance of these tripartite associations for the first time. We investigate the physiology and cytology of dual fungal symbioses in the early-diverging liverworts Allisonia and Neohodgsonia at modern and Palaeozoic-like elevated atmospheric CO2 concentrations under which they are thought to have evolved. We found enhanced carbon cost to liverworts with simultaneous Mucoromycotina and Glomeromycota associations, greater nutrient gain compared with those symbiotic with only one fungal group in previous experiments and contrasting responses to atmospheric CO2 among liverwort–fungal symbioses. In liverwort–Mucoromycotina symbioses, there is increased P-for-C and N-for-C exchange efficiency at 440 p.p.m. compared with 1500 p.p.m. CO2. In liverwort–Glomeromycota symbioses, P-for-C exchange is lower at ambient CO2 compared with elevated CO2. No characteristic cytologies of dual symbiosis were identified. We provide evidence of a distinct physiological niche for plant symbioses with Mucoromycotina fungi, giving novel insight into why dual symbioses with Mucoromycotina and Glomeromycota fungi persist to the present day.

Multigene phylogeny of Endogonales, an early diverging lineage offungi associated with plants

“…2013; Rimington et al . 2015; Field et al 2016) and a fine root endophyte (Orchard et al . 2017a) nested between the Endogone and Jimgerdemannia clades (Fig.…”

“…200 bp) so their placement will need to be revisited based on longer sequences for better resolution. Lastly, all other Endogonaceae sequences are sister to a clade of fungal sequences retrieved from the thallus of the liverwort Neohodgsonia mirabilis (Field et al 2016). …”

Bifiguratus adelaidae, gen. et sp. nov., a new member of Mucoromycotina in endophytic and soil-dwelling habitats

“…Glomeromycotina form arbuscular mycorrhizal associations, some species of Mortierellomycotina can occur with mosses and other plants (Melo et al 2014), and diverse Mucoromycotina present associations with living plants. For example, some Mucoromycotina grow on liverworts in the thallus midrib and subterranean axes (Field et al 2015a(Field et al , 2015b. Species of Umbelopsis associate with roots of orchids (Yu et al 2015), and some Mucor and Umbelopsis were isolated from woody roots of ponderosa pine and Douglas fir (Hoff et al 2004).…”

Six Key Traits of Fungi: Their Evolutionary Origins and Genetic Bases

“…The clade of AM fungi, Glomeromycotina (160), branched off approximately 400 to 450 million years ago in the phylogeny of fungi (161), and the Glomeromycotina groups with Mucoromycotina (160,162,163). This is especially interesting considering that Mucoromycotina fungi were recently shown to be mu-tualistic symbionts of basal plant groups (123,(164)(165)(166) and that hyphal structures resembling mucoralean fungi were also reported from plant fossils (167). These findings seem to change the paradigm that the Glomeromycotina was the only ancient mycorrhizal lineage.…”