The distribution and evolution of fungal symbioses in ancient lineages of land plants

An accurate understanding of the diversity and distribution of fungal symbioses in land plants is essential for mycorrhizal research. Here we update the seminal work of Wang and Qiu (Mycorrhiza 16:299-363, 2006) with a long-overdue focus on early-diverging land plant lineages, which were considerably under-represented in their survey, by examining the published literature to compile data on the status of fungal symbioses in liverworts, hornworts and lycophytes. Our survey combines data from 84 publications, including recent, post-2006, reports of Mucoromycotina associations in these lineages, to produce a list of at least 591 species with known fungal symbiosis status, 180 of which were included in Wang and Qiu (Mycorrhiza 16:299-363, 2006). Using this up-to-date compilation, we estimate that fewer than 30% of liverwort species engage in symbiosis with fungi belonging to all three mycorrhizal phyla, Mucoromycota, Basidiomycota and Ascomycota, with the last being the most widespread (17%). Fungal symbioses in hornworts (78%) and lycophytes (up to 100%) appear to be more common but involve only members of the two Mucoromycota subphyla Mucoromycotina and Glomeromycotina, with Glomeromycotina prevailing in both plant groups. Our fungal symbiosis occurrence estimates are considerably more conservative than those published previously, but they too may represent overestimates due to currently unavoidable assumptions

From rhizoids to roots? Experimental evidence of mutualism between liverworts and ascomycete fungi

Background and Aims The rhizoids of leafy liverworts (Jungermanniales, Marchantiophyta) are commonly colonized by the ascomycete fungus Pezoloma ericae. These associations are hypothesized to be functionally analogous to the ericoid mycorrhizas (ErMs) formed by P. ericae with the roots of Ericaceae plants in terms of bi-directional phosphorus for carbon exchange; however, this remains unproven. Here, we test whether associations between the leafy liverwort Cephalozia bicuspidata and P. ericae are mutualistic. Methods We measured movement of phosphorus and carbon between C. bicuspidata and P. ericae using [33P]orthophosphate and 14CO2 isotope tracers in monoxenic cultures. We also measured leafy liverwort growth, with and without P. ericae. Key Results We present the first demonstration of nutritionally mutualistic symbiosis between a non-vascular plant and an ErM-forming fungus, showing transfer of fungal-acquired P to the liverwort and of liverwort-fixed C to the fungus alongside increased growth in fungus-colonized liverworts. Conclusions Thus, this ascomycete–liverwort symbiosis can now be described as mycorrhiza-like, providing further insights into ericoid mycorrhizal evolution and adding Ascomycota fungi to mycorrhizal fungal groups engaging in mutualisms with plants across the land plant phylogeny. As P. ericae also colonizes the rhizoids of Schistochilaceae liverworts, which originated in the Triassic and are sister to all other jungermannialean liverworts associated with fungi, our findings point toward an early origin of ascomycete–liverwort symbioses, possibly pre-dating their evolution in the Ericales by some 150 million years

Lycopodiella inundata: insights into plant-fungal associations in early vascular plants

Recent studies have revealed that extant basal vascular plants associate with a wide range of Mucoromycotina and/or Glomeromycota fungi, paralleling the same in non-vascular liverworts and hornworts. This dispels the long-held paradigm that these early diverging lineages harbour Glomeromycota exclusively. Endophytes belonging to both fungal lineages have also been reported, for the first time, in a Devonian plant (Horneophyton ligneri). Together these discoveries point to much more diverse plant-fungus interactions in early vascular plants than previously assumed, however our understanding of these remains limited. In order to gain further insights into these key partnerships, especially those involving the early diverging Mucoromycotina, we are developing the lycophyte Lycopodiella inundata as an experimental system. L. inundata sporophytes have been shown to harbour solely Mucoromycotina fungi but equally fundamental, the identity of its gametophyte endophyte remains unknown. Using molecular and cytological approaches, we confirm that young L. inundata sporophytes are colonized exclusively by Mucoromycotina and show that the cytology of colonisation - consisting of both inter- and intracellular phases - closely resembles that in Haplomitriopsida liverwort-Mucoromycotina partnerships and the corm of H. ligneri. Our current isolation, resynthesis and molecular studies will provide further insights into both host and fungi specificity.This is a poster presented The Rhynie Chert – our earliest terrestrial ecosystem revisited. For more information on the conference consult the above links

Critical research challenges facing Mucoromycotina ‘fine root endophytes’

Mucoromycotina 'Fine Root Endophytes' (MFRE), referred to previously as Glomus tenue (Greenall) or more recently Planticonsortium tenue (Walker et al., 2018), are a globally distributed group of soil fungi (Orchard et al., 2017a) that form endosymbioses with plants from across most of the land plant phylogeny (Rimington et al., 2019; Hoysted et al., 2018; 2019). Despite much progress having been made in characterising plant-MFRE symbioses in the last decade, significant challenges remain

Fungal symbiont diversity drives growth of Holcus lanatusdepending on soil nutrient availability

Arbuscular mycorrhizal (AM) fungi frequently colonise plant roots and can affect plant morphology and physiology through their contribution to plant nutrition. However, the functional role of AM fungi in the presence of other microbial symbionts, including widespread Mucoromycotina ‘fine root endophytes’ (MFRE) fungi, remains largely unknown. While both AM fungi and MFRE transfer nutrients, including nitrogen, from inorganic and organic sources to host plants, their combined effects on co-colonised plants have only been investigated in liverworts. Here, we compare the morphology and physiology of the grass Holcus lanatus grown with an AM fungal community versus a more diverse symbiotic fungal community containing both AM fungi and MFRE. Holcus lanatus plants were grown in the presence of either a diverse MFRE+AM fungi soil inoculum or a multi-species AM fungal inoculum. Plant traits associated with growth were quantified, along with fungal transfer of 15N tracer to plants from a variety of sources (ammonium chloride, alanine, glycine and algal necromass). Holcus lanatus grown with the AM fungal community had greater root and shoot growth during early development and prior to the addition of 15N-labelled sources, compared with plants grown with the more diverse symbiotic fungal community. When nitrogen sources were made available to the fungal symbionts in the pot microcosms, plants growing with the MFRE+AM fungi soil inoculum had a faster growth rate than plants growing with the AM fungal community. At harvest, H. lanatus grown with the AM fungal community had a larger biomass, and there were no differences in 15N tracer assimilation in plants across the two fungal community treatments. Our results demonstrate that the diversity of fungal inocula in conjunction with soil nutrient availability determine the benefits derived by plants from diverse fungal symbionts. Our research contributes to understanding host plant outcomes in diverse multi-symbiont scenarios

Functional complementarity of ancient plant–fungal mutualisms: contrasting nitrogen, phosphorus and carbon exchanges between Mucoromycotina and Glomeromycotina fungal symbionts of liverworts

Liverworts, which are amongst the earliest divergent plant lineages and important ecosystem pioneers, often form nutritional mutualisms with arbuscular mycorrhiza‐forming Glomeromycotina and fine‐root endophytic Mucoromycotina fungi, both of which coevolved with early land plants. Some liverworts, in common with many later divergent plants, harbour both fungal groups, suggesting these fungi may complementarily improve plant access to different soil nutrients. We tested this hypothesis by growing liverworts in single and dual fungal partnerships under a modern atmosphere and under 1500 ppm [CO2], as experienced by early land plants. Access to soil nutrients via fungal partners was investigated with 15N‐labelled algal necromass and 33P orthophosphate. Photosynthate allocation to fungi was traced using 14CO2. Only Mucoromycotina fungal partners provided liverworts with substantial access to algal 15N, irrespective of atmospheric CO2 concentration. Both symbionts increased 33P uptake, but Glomeromycotina were often more effective. Dual partnerships showed complementarity of nutrient pool use and greatest photosynthate allocation to symbiotic fungi. We show there are important functional differences between the plant–fungal symbioses tested, providing new insights into the functional biology of Glomeromycotina and Mucoromycotina fungal groups that form symbioses with plants. This may explain the persistence of the two fungal lineages in symbioses across the evolution of land plants

A mycorrhizal revolution.

It has long been postulated that symbiotic fungi facilitated plant migrations onto land through enhancing the scavenging of mineral nutrients and exchanging these for photosynthetically fixed organic carbon. Today, land plant-fungal symbioses are both widespread and diverse. Recent discoveries show that a variety of potential fungal associates were likely available to the earliest land plants, and that these early partnerships were probably affected by changing atmospheric CO2 concentrations. Here, we evaluate current hypotheses and knowledge gaps regarding early plant-fungal partnerships in the context of newly discovered fungal mutualists of early and more recently evolved land plants and the rapidly changing views on the roles of plant-fungal symbioses in the evolution and ecology of the terrestrial biosphere

Mucoromycotina fine root endophyte fungi form nutritional mutualisms with vascular plants

Fungi and plants have engaged in intimate symbioses that are globally widespread and have driven terrestrial biogeochemical processes since plant terrestrialization >500 million years ago. Recently, hitherto unknown nutritional mutualisms involving ancient lineages of fungi and nonvascular plants have been discovered, although their extent and functional significance in vascular plants remain uncertain. Here, we provide evidence of carbon-for-nitrogen exchange between an early-diverging vascular plant (Lycopodiella inundata) and Mucoromycotina (Endogonales) fine root endophyte fungi. Furthermore, we demonstrate that the same fungal symbionts colonize neighboring nonvascular and flowering plants. These findings fundamentally change our understanding of the physiology, interrelationships, and ecology of underground plant–fungal symbioses in modern terrestrial ecosystems by revealing the nutritional role of Mucoromycotina fungal symbionts in vascular plants

Ancient plants with ancient fungi: liverworts associate with early-diverging arbuscular mycorrhizal fungi

Arbuscular mycorrhizas are widespread in land plants including liverworts, some of the closest living relatives of the first plants to colonize land 500 million years ago (MYA). Previous investigations reported near-exclusive colonization of liverworts by the most recently evolved arbuscular mycorrhizal fungi, the Glomeraceae, indicating a recent acquisition from flowering plants at odds with the widely held notion that arbuscular mycorrhizal-like associations in liverworts represent the ancestral symbiotic condition in land plants. We performed an analysis of symbiotic fungi in 674 globally collected liverworts using molecular phylogenetics and electron microscopy. Here, we show every order of arbuscular mycorrhizal fungi colonizes early-diverging liverworts, with non-Glomeraceae being at least 10 times more common than in flowering plants. Arbuscular mycorrhizal fungi in liverworts and other ancient plant lineages (hornworts, lycopods, and ferns) were delimited into 58 taxa and 36 singletons, of which at least 43 are novel and specific to liverworts. The discovery that early plant lineages are colonized by early-diverging fungi supports the hypothesis that arbuscular mycorrhizas are an ancestral symbiosis for all land plants