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Endogonales (Mucoromycotina), composed of Endogonaceae and Densosporaceae, is the only known non-Dikarya order with ectomycorrhizal members. They also form mycorrhizal-like association with some nonspermatophyte plants. It has been recently proposed that Endogonales were among the earliest mycorrhizal partners with land plants. It remains unknown whether Endogonales possess genomes with mycorrhizal-lifestyle signatures and whether Endogonales originated around the same time as land plants did. We sampled sporocarp tissue from four Endogonaceae collections and performed shotgun genome sequencing. After binning the metagenome data, we assembled and annotated the Endogonaceae genomes. We performed comparative analysis on plant-cell-wall-degrading enzymes (PCWDEs) and small secreted proteins (SSPs). We inferred phylogenetic placement of Endogonaceae and estimated the ages of Endogonaceae and Endogonales with expanded taxon sampling. Endogonaceae have large genomes with high repeat content, low diversity of PCWDEs, but without elevated SSP/secretome ratios. Dating analysis estimated that Endogonaceae originated in the Permian-Triassic boundary and Endogonales originated in the mid-late Silurian. Mycoplasma-related endobacterium sequences were identified in three Endogonaceae genomes. Endogonaceae genomes possess typical signatures of mycorrhizal lifestyle. The early origin of Endogonales suggests that the mycorrhizal association between Endogonales and plants might have played an important role during the colonization of land by plants.

Some soil fungi in the Leotiomycetes form ericoid mycorrhizal (ERM) symbioses with Ericaceae. In the harsh habitats in which they occur, ERM plant survival relies on nutrient mobilization from soil organic matter (SOM) by their fungal partners. The characterization of the fungal genetic machinery underpinning both the symbiotic lifestyle and SOM degradation is needed to understand ERM symbiosis functioning and evolution, and its impact on soil carbon (C) turnover. We sequenced the genomes of the ERM fungi Meliniomyces bicolor, M. variabilis, Oidiodendron maius and Rhizoscyphus ericae, and compared their gene repertoires with those of fungi with different lifestyles (ecto- and orchid mycorrhiza, endophytes, saprotrophs, pathogens). We also identified fungal transcripts induced in symbiosis. The ERM fungal gene contents for polysaccharide-degrading enzymes, lipases, proteases and enzymes involved in secondary metabolism are closer to those of saprotrophs and pathogens than to those of ectomycorrhizal symbionts. The fungal genes most highly upregulated in symbiosis are those coding for fungal and plant cell wall-degrading enzymes (CWDEs), lipases, proteases, transporters and mycorrhiza-induced small secreted proteins (MiSSPs). The ERM fungal gene repertoire reveals a capacity for a dual saprotrophic and biotrophic lifestyle. This may reflect an incomplete transition from saprotrophy to the mycorrhizal habit, or a versatile life strategy similar to fungal endophytes.

Soil depth partitioning is thought to promote the diversity of ectomycorrhizal ( EM) fungal communities, but little is known about whether it is controlled by abiotic or biotic factors., In three bioassay experiments, we tested the role of vertical soil heterogeneity in determining the distributions and competitive outcomes of the EM sister species Rhizopogon vinicolor and Rhizopogon vesiculosus. We planted Pseudotsuga menziesii seedlings into soils that were either a homogenized mix of upper and lower depths or vertically stratified combinations mimicking natural field conditions., We found that both species colonized the upper or lower soil depths in the absence of competition, suggesting that their distributions were not limited by abiotic edaphic factors. In competition within homogeneous soils, R. vesiculosus completely excluded colonization by R. vinicolor, but R. vinicolor was able to persist when soils were stratified. The amount of colonization by R. vinicolor in the stratified soils was also significantly correlated with the number of multilocus genotypes present., Taken together, our findings suggest that the differential vertical distributions of R. vinicolor and R. vesiculosus in natural settings are probably attributable to competition rather than edaphic specialization, but that soil heterogeneity may play a key role in promoting EM fungal diversity. [ABSTRACT FROM AUTHOR]

Mixia osmundae ( Basidiomycota, Pucciniomycotina) represents a monotypic class containing an unusual fern pathogen with incompletely understood biology. We sequenced and analyzed the genome of M. osmundae, focusing on genes that may provide some insight into its mode of pathogenicity and reproductive biology., Mixia osmundae has the smallest plant pathogenic basidiomycete genome sequenced to date, at 13.6 Mb, with very few repeats, high gene density, and relatively few significant gene family gains., The genome shows that the yeast state of M. osmundae is haploid and the lack of segregation of mating genes suggests that the spores produced on Osmunda spp. fronds are probably asexual. However, our finding of a complete complement of mating and meiosis genes suggests the capacity to undergo sexual reproduction. Analyses of carbohydrate active enzymes suggest that this fungus is a biotroph with the ability to break down several plant cell wall components., Analyses of publicly available sequence data show that other Mixia members may exist on other plant hosts and with a broader distribution than previously known. [ABSTRACT FROM AUTHOR]

• We have developed microsatellite markers for two sister species of Rhizopogon, R. vesiculosus and R. vinicolor (Boletales, Basidiomycota), and used selected markers to investigate genet size and distribution from ectomycorrhizal samples. Both species form ectomycorrhizas with tuberculate morphology on Douglas-fir ( Pseudotsuga menziesii). • Tuberculate ectomycorrhizas were sampled and mapped in two 10 × 10 m core plots located at Mary's Peak in the Oregon Coast Range and at Mill Creek in the Oregon Cascade Mountains, USA; additional samples were obtained from a larger area surrounding the Mary's Peak core plot. • Gene diversities at the newly described microsatellite loci ranged from 0.00 to 0.68 in R. vesiculosus, and from 0.00 to 0.43 in R. vinicolor. Both taxa appeared to be in Hardy–Weinberg and linkage equilibrium. The largest distance observed between tuberculate ectomycorrhizas of the same genet was 13.4 m for R. vesiculosus, but only 2 m for R. vinicolor. • This is to our knowledge the first study to differentiate fungal genets from ectomycorrhizas with great confidence using multiple codominant markers. [ABSTRACT FROM AUTHOR]

We aimed to identify genomic traits of transitions to ectomycorrhizal ecology within the Boletales by comparing the genomes of 21 symbiotrophic species with their saprotrophic brown-rot relatives. Gene duplication rate is constant along the backbone of Boletales phylogeny with large loss events in several lineages, while gene family expansion sharply increased in the late Miocene, mostly in the Boletaceae. Ectomycorrhizal Boletales have a reduced set of plant cell-wall-degrading enzymes (PCWDEs) compared with their brown-rot relatives. However, the various lineages retain distinct sets of PCWDEs, suggesting that, over their evolutionary history, symbiotic Boletales have become functionally diverse. A smaller PCWDE repertoire was found in Sclerodermatineae. The gene repertoire of several lignocellulose oxidoreductases (e.g. laccases) is similar in brown-rot and ectomycorrhizal species, suggesting that symbiotic Boletales are capable of mild lignocellulose decomposition. Transposable element (TE) proliferation contributed to the higher evolutionary rate of genes encoding effector-like small secreted proteins, proteases, and lipases. On the other hand, we showed that the loss of secreted CAZymes was not related to TE activity but to DNA decay. This study provides novel insights on our understanding of the mechanisms influencing the evolutionary diversification of symbiotic boletes., (© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.)