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

Abstract

Endogonales is a lineage of early diverging fungi within Mucoromycota. Many species in this order produce small sporophores (“sporocarps”) containing a large number of zygospores, and many species form symbioses with plants. However, due to limited collections, subtle morphological differentiation, difficulties in growing these organisms in vitro, and idiosyncrasies in their rDNA that make PCR amplification difficult, the systematics and character evolution of these fungi have been challenging to resolve. To overcome these challenges we generated a multigene phylogeny of Endogonales using sporophores collected over the past three decades from four continents. Our results show that Endogonales harbour significant undescribed diversity and form two deeply divergent and well-supported phylogenetic clades, which we delimit as the families Endogonaceae and Densosporaceae fam. nov. The family Densosporaceae consists of the genus Densospora, Sphaerocreas pubescens, and many diverse lineages known only from environmental DNA sequences of plant-endosymbiotic fungi. Within Endogonaceae there are two clades. One corresponds to Endogone and includes the type species, E. pisiformis. Species of Endogone are characterized by above- and below-ground sporophores, a hollow and infolded sporophore form, a loose zygosporangial hyphal mantle, homogeneous gametangia, and an enigmatic trophic mode with no evidence of ectomycorrhizal association for most species. For the other clade we introduce a new generic name, Jimgerdemannia gen. nov. Members of that genus (J. flammicorona and J. lactiflua species complexes, and an undescribed species) are characterized by hypogeous sporophores with a solid gleba, a well-developed zygosporangial hyphal mantle, heterogeneous gametangia, and an ectomycorrhizal trophic mode. Future studies on Densosporaceae and Endogonaceae will be important for understanding fungal innovations including evolution of macroscopic sporophores and symbioses with plants.

Evidence for Co-evolutionary History of Early Diverging Lycopodiaceae Plants With Fungi

“…Independent calibrated molecular dating studies that include Endogonales, AMF, and other early diverging lineages indicate that Endogonales originate in the mid-late Silurian (∼420 Ma), contemporaneously with AMF and lycopods (Lutzoni et al, 2018;Chang et al, 2019). Phylogenetic systematics of Endogonales have resolved two family level clades: Endogonaceae and Densosporaceae (Desirò et al, 2017). Endogonaceae consists of Endogone and Jimgerdemannia, two deeply divergent monophyletic lineages of macro sporocarp producing species, that differ in spore morphology, sporing habit, and (putatively) ecology.…”

“…However, the identification of other fungal associations in Mucoromycotina with early land plant lineages and new fungal fossils has sparked great interest in the origin of plant-fungal associations (Desirò et al, 2013(Desirò et al, , 2015Truong et al, 2017). Recent identification of Endogonales and other Mucoromycotina symbioses in vascular, non-vascular, and fossil plants suggest there is also an ancient relationship between land plants and some cryptic Mucoromycotina fungi (Field et al, 2015;Rimington et al, 2015;Desirò et al, 2017;Strullu-Derrien et al, 2018).…”

Fungal evolution: diversity, taxonomy and phylogeny of the Fungi

“…Recent phylogenetic studies based on 18S rRNA place the genus Sphaerocreas as a sister branch to a group of uncultured symbionts of liverworts, forming a distinct lineage within Mucoromycotina (Hirose et al ., ; Benny et al ., ). Densospora (McGee, ) is an ectomycorrhizal fungus isolated from Australia that contains several morphological traits that suggest ambiguous affiliation to either Endogonales or Glomeromycota (Gleason & McGee, ; Desirò et al ., ). A multigene phylogeny recovered an affiliation between Sphaerocreas and Densospora – a relationship that should further be explored in the near future (Desirò et al ., ).…”

“…Densospora (McGee, ) is an ectomycorrhizal fungus isolated from Australia that contains several morphological traits that suggest ambiguous affiliation to either Endogonales or Glomeromycota (Gleason & McGee, ; Desirò et al ., ). A multigene phylogeny recovered an affiliation between Sphaerocreas and Densospora – a relationship that should further be explored in the near future (Desirò et al ., ). Bifiguratus is a recently described fungus with an endophytic and saprotrophic lifestyle that appears as a distinct and early‐splitting lineage within the Mucoromycotina (Torres‐Cruz et al ., ).…”

Dual‐mycorrhizal plants: their ecology and relevance

“…As the land masses evolved and ecosystems developed along with pedogenesis, so did other fungi. At c. 190 Ma, multiple groups of saprotrophic fungi, such as brown-and white-rot fungi (Skrede et al, 2011;Floudas et al, 2012) from the Basidiomycota, Ascomycota, and Endogonales from the Mucoromycotina (Desir o et al, 2017) began to form a new type of association, primarily with gymnosperm trees species (e.g. Gnetum spp.).…”