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Studying the signatures of evolution can help to understand genetic processes. Here, we demonstrate how the existence of balancing selection can be used to identify the breeding systems of fungi from genomic data. The breeding systems of fungi are controlled by self-incompatibility loci that determine mating types between potential mating partners, resulting in strong balancing selection at the loci. Within the fungal phylum Basidiomycota, two such self-incompatibility loci, namely HD MAT locus and P/R MAT locus, control mating types of gametes. Loss of function at one or both MAT loci results in different breeding systems and relaxes the MAT locus from balancing selection. By investigating the signatures of balancing selection at MAT loci, one can infer a species’ breeding system without culture-based studies. Nevertheless, the extreme sequence divergence among MAT alleles imposes challenges for retrieving full variants from both alleles when using the conventional read-mapping method. Therefore, we employed a combination of read-mapping and local de novo assembly to construct haplotypes of HD MAT alleles from genomes in suilloid fungi (genera Suillus and Rhizopogon). Genealogy and pairwise divergence of HD MAT alleles showed that the origins of mating types predate the split between these two closely related genera. High sequence divergence, trans-specific polymorphism, and the deeply diverging genealogy confirm the long-term functionality and multiallelic status of HD MAT locus in suilloid fungi. This work highlights a genomics approach to studying breeding systems regardless of the culturability of organisms based on the interplay between evolution and genetics.

Gene copy number variation across individuals has been shown to track population structure and be a source of adaptive genetic variation with significant fitness impacts. In this study, we report opposite results for both predictions based on the analysis of gene copy number variants (CNVs) of Suillus brevipes, a mycorrhizal fungus adapted to coastal and montane habitats in California. In order to assess whether gene copy number variation mirrored population structure and selection in this species, we investigated two previously studied locally adapted populations showing a highly differentiated genomic region encompassing a gene predicted to confer salt tolerance. In addition, we examined whether copy number in the genes related to salt homeostasis was differentiated between the two populations. Although we found many instances of CNV regions across the genomes of S. brevipes individuals, we also found CNVs did not recover population structure and known salt-tolerance-related genes were not under selection across the coastal population. Our results contrast with predictions of CNVs matching single-nucleotide polymorphism divergence and showed CNVs of genes for salt homeostasis are not under selection in S. brevipes.

Recombination suppression on sex chromosomes often extends in a stepwise manner, generating evolutionary strata of differentiation between sex chromosomes. Sexual antagonism is a widely accepted explanation for evolutionary strata, postulating that sets of genes beneficial in only one sex are successively linked to the sex-determining locus. The anther-smut fungus Microbotryum lychnidis-dioicae has mating-type chromosomes with evolutionary strata, only some of which link mating-type genes. Male and female roles are non-existent in this fungus, but mating-type antagonistic selection can also generate evolutionary strata, although the life cycle of the fungus suggests it should be restricted to few traits. Here, we tested the hypothesis that mating-type antagonism may have triggered recombination suppression beyond mating-type genes in M. lychnidis-dioicae by searching for footprints of antagonistic selection in evolutionary strata not linking mating-type loci. We found that these evolutionary strata (i) were not enriched in genes upregulated in the haploid phase, where cells are of alternative mating types, (ii) carried no gene differentially expressed between mating types, and (iii) carried no genes displaying footprints of specialization in terms of protein sequences (dN/dS) between mating types after recommended filtering. Without filtering, eleven genes showed signs of positive selection in the strata not linking mating-type genes, which constituted an enrichment compared to autosomes, but their functions were not obviously involved in antagonistic selection. Thus, we found no strong evidence that antagonistic selection has contributed to extending recombination suppression beyond mating-type genes. Alternative hypotheses should therefore be explored to improve our understanding of the sex-related chromosome evolution.

Geothermal soils offer unique insight into the way extreme environmental factors shape communities of organisms. However, little is known about the fungi growing in these environments and in particular how localized steep abiotic gradients affect fungal diversity. We used metabarcoding to characterize soil fungi surrounding a hot spring-fed thermal creek with water up to 84 °C and pH 10 in Yellowstone National Park. We found a significant association between fungal communities and soil variable principal components, and we identify the key trends in co-varying soil variables that explain the variation in fungal community. Saprotrophic and ectomycorrhizal fungi community profiles followed, and were significantly associated with, different soil variable principal components, highlighting potential differences in the factors that structure these different fungal trophic guilds. In addition, in vitro growth experiments in four target fungal species revealed a wide range of tolerances to pH levels but not to heat. Overall, our results documenting turnover in fungal species within a few hundred meters suggest many co-varying environmental factors structure the diverse fungal communities found in the soils of Yellowstone National Park.

Geothermal soils offer unique insight into the way extreme environmental factors shape communities of organisms. However, little is known about the fungi growing in these environments and in particular how localized steep abiotic gradients affect fungal diversity. We used metabarcoding to characterize soil fungi surrounding a hot spring-fed thermal creek with water up to 84 °C and pH 10 in Yellowstone National Park. We found a significant association between fungal communities and soil variable principal components, and we identify the key trends in co-varying soil variables that explain the variation in fungal community. Saprotrophic and ectomycorrhizal fungi community profiles followed, and were significantly associated with, different soil variable principal components, highlighting potential differences in the factors that structure these different fungal trophic guilds. In addition, in vitro growth experiments in four target fungal species revealed a wide range of tolerances to pH levels but not to heat. Overall, our results documenting turnover in fungal species within a few hundred meters suggest many co-varying environmental factors structure the diverse fungal communities found in the soils of Yellowstone National Park.

Recent research provides an unprecedented account of the diversity and biomass of life, but the data also suggest unexplained patterns such as the co-dominance of very different life forms. We compile the planetary body size biomass spectrum across all taxa and investigate possible underlying forces. We find that small (10-14 g) and large (106 g) organisms vastly outweigh other sizes. The global spectrum reveals an allometric power exponent close to zero, with the marine spectrum in particular showing multiple closely packed modes that are compatible with metabolic food webs. All habitat realms share two distinct size modes that correspond well to the evolutionary innovations of unicellular and complex multicellular life forms, plus a smaller third mode representing unicellular endosymbiotic life. Each mode contains both producers and consumers. These findings show both differences and similarities across habitat realms and point to a size-based synthesis of microevolution, macroevolution, and macroecology.

This is the sixth in a series of papers where we bring collaborating mycologists together to produce a set of notes of several taxa of fungi. In this study we introduce a new family Fuscostagonosporaceae in Dothideomycetes. We also introduce the new ascomycete genera Acericola, Castellaniomyces, Dictyosporina and Longitudinalis and new species Acericola italica, Alternariaster trigonosporus, Amarenomyces dactylidis, Angustimassarina coryli, Astrocystis bambusicola, Castellaniomyces rosae, Chaetothyrina artocarpi, Chlamydotubeufia krabiensis, Colletotrichum lauri, Collodiscula chiangraiensis, Curvularia palmicola, Cytospora mali-sylvestris, Dictyocheirospora cheirospora, Dictyosporina ferruginea, Dothiora coronillae, Dothiora spartii, Dyfrolomyces phetchaburiensis, Epicoccum cedri, Epicoccum pruni, Fasciatispora calami, Fuscostagonospora cytisi, Grandibotrys hyalinus, Hermatomyces nabanheensis, Hongkongmyces thailandica, Hysterium rhizophorae, Jahnula guttulaspora, Kirschsteiniothelia rostrata, Koorchalomella salmonispora, Longitudinalis nabanheensis, Lophium zalerioides, Magnibotryascoma mali, Meliola clerodendri-infortunati, Microthyrium chinense, Neodidymelliopsis moricola, Neophaeocryptopus spartii, Nigrograna thymi, Ophiocordyceps cossidarum, Ophiocordyceps issidarum, Ophiosimulans plantaginis, Otidea pruinosa, Otidea stipitata, Paucispora kunmingense, Phaeoisaria microspora, Pleurothecium floriforme, Poaceascoma halophila, Periconia aquatica, Periconia submersa, Phaeosphaeria acaciae, Phaeopoacea muriformis, Pseudopithomyces kunmingnensis, Ramgea ozimecii, Sardiniella celtidis, Seimatosporium italicum, Setoseptoria scirpi, Torula gaodangensis and Vamsapriya breviconidiophora. We also provide an amended account of Rhytidhysteron to include apothecial ascomata and a J+ hymenium. The type species of Ascotrichella hawksworthii (Xylariales genera incertae sedis), Biciliopsis leptogiicola (Sordariomycetes genera incertae sedis), Brooksia tropicalis (Micropeltidaceae), Bryochiton monascus (Teratosphaeriaceae), Bryomyces scapaniae (Pseudoperisporiaceae), Buelliella minimula (Dothideomycetes genera incertae sedis), Carinispora nypae (Pseudoastrosphaeriellaceae), Cocciscia hammeri (Verrucariaceae), Endoxylina astroidea (Diatrypaceae), Exserohilum turcicum (Pleosporaceae), Immotthia hypoxylon (Roussoellaceae), Licopolia franciscana (Vizellaceae), Murispora rubicunda (Amniculicolaceae) and Doratospora guianensis (synonymized under Rizalia guianensis, Trichosphaeriaceae) were re-examined and descriptions, illustrations and discussion on their familial placement are given based on phylogeny and morphological data. New host records or new country reports are provided for Chlamydotubeufia huaikangplaensis, Colletotrichum fioriniae, Diaporthe subclavata, Diatrypella vulgaris, Immersidiscosia eucalypti, Leptoxyphium glochidion, Stemphylium vesicarium, Tetraploa yakushimensis and Xepicula leucotricha. Diaporthe baccae is synonymized under Diaporthe rhusicola. A reference specimen is provided for Periconia minutissima. Updated phylogenetic trees are provided for most families and genera. We introduce the new basidiomycete species Agaricus purpurlesquameus, Agaricus rufusfibrillosus, Lactifluus holophyllus, Lactifluus luteolamellatus, Lactifluus pseudohygrophoroides, Russula benwooii, Russula hypofragilis, Russula obscurozelleri, Russula parapallens, Russula phoenicea, Russula pseudopelargonia, Russula pseudotsugarum, Russula rhodocephala, Russula salishensis, Steccherinum amapaense, Tephrocybella constrictospora, Tyromyces amazonicus and Tyromyces angulatus and provide updated trees to the genera. We also introduce Mortierella formicae in Mortierellales, Mucoromycota and provide an updated phylogenetic tree. Fil: Hyde, Kevin D.. Mae Fah Luang University. Center Of Excellence In Fungal Research; Tailandia Fil: Norphanphoun, Chada. Mae Fah Luang University. Center Of Excellence In Fungal Research; Tailandia Fil: Abreu, Vanessa P.. Universidade Federal de Viçosa; Brasil Fil: Bazzicalupo, Anna. University of British Columbia; Canadá Fil: Thilini Chethana, K. W.. Mae Fah Luang University. Center Of Excellence In Fungal Research; Tailandia Fil: Romero, Andrea Irene. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Micología y Botánica. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Micología y Botánica; Argentina Fil: Liu, Jian-Kui. Guizhou Academy of Agricultural Sciences; China Fil: Liu, Zuo-Yi. Guizhou Academy of Agricultural Sciences; China Fil: Longoni Plautz Jr., Helio. Instituto de Ciências Biológicas; Brasil Fil: Lumyong, Saisamorn. Chiang Mai University; Tailandia Fil: Maharachchikumbura, Sajeewa S. N.. Sultan Qaboos University; Omán Fil: Matočec, Neven. Ruđer Bošković Institute; Croacia Fil: McKenzie, Eric H. C.. Landcare Research Manaaki Whenua; Nueva Zelanda Fil: Mešić, Armin. Ruđer Bošković Institute; Croacia Fil: Miller, Daniel. Puget Sound Mycological Society; Estados Unidos Fil: Pawłowska, Julia. University of Warsaw; Polonia Fil: Pereira, Olinto L.. Universidade Federal de Viçosa; Brasil Fil: Promputtha, Itthayakorn. Mae Fah Luang University; Tailandia Fil: Ryvarden, Leif. University of Oslo; Noruega Fil: Su, Hong-Yan. Dali University; China Fil: Suetrong, Satinee. National Center for Genetic Engineering and Biotechnology; Tailandia Fil: Tkalčec, Zdenko. Ruđer Bošković Institute; Croacia Fil: Vizzini, Alfredo. Università di Torino; Italia Fil: Wen,Ting-Chi. Guizhou University; China Fil: Wisitrassameewong, Komsit. Seoul National University; Corea del Sur Fil: Wrzosek, Marta. University of Warsaw; Polonia Fil: Xu, Jian-Chu. Mae Fah Luang University; Tailandia Fil: Zhao, Qi. Chinese Academy of Sciences; República de China Fil: Zhao, Rui-Lin. Chinese Academy of Sciences; República de China Fil: Mortimer, Peter E.. Chinese Academy of Sciences; República de China

Human-altered environments can shape the evolution of organisms. Fungi are no exception, though little is known about how they withstand anthropogenic pollution. Here, we document incipient polygenic local adaptation in the mycorrhizal fungus Suillus luteus driven by recent soil heavy metal contamination. Genome scans across individuals from recently polluted and nearby unpolluted soils in Belgium revealed no evidence of population structure but detected allelic divergence and gene copy number variation in genes involved in metal exclusion, storage, immobilization, and reactive oxygen species detoxification. Standing genetic variation included multiple alleles of small effects contributing to heavy metal tolerance, suggesting the existence of different strategies to withstand contamination. These variants were shared across the whole population but under selection in isolates exposed to pollution. Together, our results point to S. luteus undergoing the initial steps of adaptive divergence and contribute to understanding the processes underlying local adaptation under strong environmental selection.

Some but not all of the species of ’little brown mushrooms’ in the genus Galerina contain deadly amatoxins at concentrations equaling those in the death cap, Amanita phalloides. However, Galerina’s ~300 species are notoriously difficult to identify by morphology, and the identity of toxin-containing specimens has not been verified with DNA barcode sequencing. This left open the question of which Galerina species contain toxins and which do not. We selected specimens for toxin analysis using a preliminary phylogeny of the fungal DNA barcode region, the ribosomal internal transcribed spacer (ITS) region. Using liquid chromatography/mass spectrometry, we analyzed amatoxins from 70 samples of Galerina and close relatives, collected in western British Columbia, Canada. To put the presence of toxins into a phylogenetic context, we included the 70 samples in maximum likelihood analyses of 438 taxa, using ITS, RNA polymerase II second largest subunit gene (RPB2), and nuclear large subunit ribosomal RNA (LSU) gene sequences. We sequenced barcode DNA from types where possible to aid with applications of names. We detected amatoxins only in the 24 samples of the G. marginata s.l. complex in the Naucoriopsis clade. We delimited 56 putative Galerina species using Automatic Barcode Gap Detection software. Phylogenetic analysis showed moderate to strong support for Galerina infrageneric clades Naucoriopsis, Galerina, Tubariopsis, and Sideroides. Mycenopsis appeared paraphyletic and included Gymnopilus. Amatoxins were not detected in 46 samples from Galerina clades outside of Naucoriopsis or from outgroups. Our data show significant quantities of toxin in all mushrooms tested from the G. marginata s.l. complex. DNA barcoding revealed consistent accuracy in morphology-based identification of specimens to G. marginata s.l. complex. Prompt and careful morphological identification of ingested G. marginata s.l. has the potential to improve patient outcomes by leading to fast and appropriate treatment.

In this commentary, we discuss evidence for the phylogenetic affiliations of Tortotubus protuberans, the subject of Martin Smith's 2016 paper in the Botanical Journal of the Linnean Society entitled, ‘Cord-forming Palaeozoic fungi in terrestrial assemblages’. We agree that the fossilized, branching, somatic filaments probably represent fungal hyphae. We were not convinced by Smith's proposal that T. protuberans represents Dikarya, the clade of fungi that includes most modern moulds, yeasts and mushrooms. To justify classification, Smith relied on structures that are analogous between T. protuberans and modern fungi, and argued ‘that Dikarya can produce the range of morphologies expressed by T. protuberans’. We review available information about homologies of the characteristics of T. protuberans, including mycelial cords, retrograde growth, septal pores and ornamented hyphae. Retrograde growth in T. protuberans is intriguing from an evolutionary developmental point of view, but it differs sufficiently in fine detail when compared with growth patterns in croziers or clamp connections of Dikarya, so that homologies are unclear. Tortotubus protuberans is an important fossil form, but we suggest taking a step back and relating it to the distribution of character evolution through the fungal phylogeny rather than to derived characters of modern taxa.