Examining the macro-evolution and genetic background of complex multicellular structures in mushroom-forming fungi (Agaricomycetes)

Several major transitions have happened through the evolution of life, such as the evolution of eukaryotes, plastids, or multicellularity. Multicellular organisms exist in all biogeographic realms and are essential components of most present ecosystems. Simple multicellular organisms form aggregates or colonies of cells and have arisen in both prokaryotic and eukaryotic lineages at least 25 times. In contrast, complex multicellularity, where three-dimensional structures are developed and only some of their cells are in direct contact with the environment, evolved exclusively in five eukaryotic lineages from which three dominate the present terrestrial ecosystems: animals, embryophytic land plants and fungi. Despite the prevalence of complex multicellularity on Earth, the driving force and the genetic background of the evolution of complex multicellular organisms are incompletely known. Both biotic and abiotic factors could drive the evolution of complex multicellularity such as changes in feeding mode, increase in atmospheric oxygen, or whole-genome duplications. Pieces of evidence also mount that the evolution of multicellular organisms was driven by exaptation, a mechanism where a pre-existing genetic toolkit of ancestors can give new adaptive features for descendants. The fungal kingdom is one of the five main groups where complex multicellularity evolved, but complex multicellularity could have convergently appeared at least eight times within fungi. The convergent evolution of complex multicellularity in the fungal kingdom implies a unique evolutionary solution for developing complex structures. Fungal complex multicellular structures are bound to a particular life period (fruiting bodies) or circumstances (mycorrhizae, rhizomorphs), and these are only a part of the whole organism. In contrast to this, the whole individual is the complex multicellular entity in other complex multicellular organisms. Possibly, the most common fungal complex multicellular structures are the sexual fruiting bodies, whose primary purpose is to produce meiotic spores in a protective environment and facilitate spore dispersal. Agaricomycetes, also called mushroom-forming fungi, contain more than 20,000 species, which produce fruiting bodies. Therefore, examining this class of fungi with phylogenetic comparative methods (PCMs) would widen our knowledge on the macro-evolution of complex morphologies in fungi. Previous studies have examined small datasets or separate Agaricomycetes taxa using PCMs. So far, it is revealed that the evolution of mushrooms could have started as a resupinate ancestor (crust-like fruiting body) and through a coralloid/clavarioid type, pileate-stipitate mushrooms (fruiting body with cap and stipe) convergently evolved. It was also showed that pileate-stipitate fruiting bodies could increase the diversification rate of lineages, indicating that this morphology bears advantageous traits for species. However, the global evolutionary history of the Agaricomycetes and some of the key traits of pileate-stipitate mushrooms (presence of cap, protecting veils, structured hymenophore) have not been examined using sufficiently large and robust data. Therefore, we gathered specimens of Agaricomycetes from every geographical region except Antarctica and assembled a dataset containing 5,284 species and three genomic loci (nrLSU, rpb2, tef1-α). Using this dataset, we performed maximum likelihood (ML) inference, and we constrained the topology of the backbone based on a phylogenomic tree consist of 105 species. Overall, 245 ML trees were inferred, covering the topological variety of Agaricomycetes phylogeny based on Robinson-Foulds pairwise distances. We also performed molecular clock calibration on ten trees selected by stratified random sampling to represent the topology diversity of the 245 trees. The molecular clock calibration was done by a two-step time calibration strategy. This procedure was based on using a robust and precise method on the ten percent of the species to infer parameters. Then, the time calibration of trees with all species was performed using a less precise but a fast algorithm to which the parameters inferred in the first step was inputted. Most of the order-level clades were dated to the Jurassic period (200-145 Ma ago), including the two subclasses Agaricomycetidae and Phallomycetidae. These ages are older than the time estimates of previous studies, therefore we tried to disentangle the underlying causes by reconstructing time-calibrated phylogenomic trees with various settings to perform a sensitivity analysis. Overall, we found that the precise placement of fossil calibration point on the phylogeny has the most significant effect on age estimates, and the number of fossil calibration points, the type of the tree (phylogenetic vs. phylogenomic) and the software choice have a smaller effect on the result of the time calibration. Therefore, we think our analyses provide a robust and st

Mycorrhizal colonization by Tuber aestivum has a negative effect on the vitality of oak and hazel seedlings

Ectomycorrhizal fungi have a great impact on the ecosystem in boreal and temperate regions, and it has commercial, silvicultural and crop importance as well. The summer truffle (Tuber aestivum), a common mycorrhizal partner of several trees, is a valuable ectomycorrhizal fungus since its fruit bodies (ascomata) are a popular and expensive product on the global markets. To understand the physiology and ecology of a natural forest or a plantation, the participants and relationships between them should be examined. Hence, the maximal quantum efficiency of photosystem II centers, that is vitality of half a year old oak (Quercus robur) and hazel (Corylus avellana) seedlings inoculated with summer truffle was measured. The relation between the vitality of the plants and the rate of colonization of the fungus was examined applying single and multiple linear regressions. In the case of the oak seedlings contamination of Scleroderma spp. morphotype colonization was observed. Negative relationship between rate of colonization and the vitality was detected in the case of hazel seedling and non-contaminated oak seedlings. Multiple linear regression analysis revealed that there is no effect of truffle and contaminant fungi together, but alone the truffle has a negative impact. Consequently, the Scleroderma ectomycorrhiza seemed to have a balancing effect on the negative impact of summer truffle

Changes of hypogeous funga in the Carpathian-Pannonian region in the past centuries

The exploration of hypogeous fungi in the Carpathian-Pannonian region speeded up in the past decades, owing to the widespread of truffle hunting with dogs. As a result, not only several new species were found in the region, but our view of the frequency of truffles also changed fundamentally. It became evident that Tuber aestivum, T. brumale, T. macrosporum, T. magnatum, T. mesentericum and Mattirolomyces terfezioides can be collected in commercial quantity. Among the dog preferred hypogeous fungi (DPH) several species, earlier believed to be rare like Octaviania asterosperma and Stephensia bombycina, also occurred. The taxonomic alterations and revisions brought about changes in the list of hypogeous fungi, and further changes are expected from molecular taxonomy research on a number of genera at present

Sixty-one macrofungi species new to Hungary in Őrség National Park

In this paper, an annotated checklist of macrofungi from Őrség National Park, West Hungary, is provided. A total of 726 macrofungi taxa representing 214 genera, 84 classes and 2 phyla (Asco- and Basidiomycota) were revealed. Sixty-one macrofungi species were new to the mycobiota of Hungary. Sporocarps were collected three times (in May, August and September–October) between 2009 and 2010 in 35 (40 m × 40 m) forest stands with different tree species compositions. Preferred tree species compositions and substrata of registered macrofungi are also listed

Comparative and phylogenomic analysis of nuclear and organelle genes in cryptic Coelastrella vacuolata MACC-549 green algae

The nuclear, chloroplast and mitochondrial genomes of a unicellular green algal species of the Coelastrella genus was sequenced, assembled and annotated. The strain was previously classified as Chlamydomonas sp. MACC-549 based on morphology and partial 18S rDNA analysis. However, the proposed multi-loci phylogenomic approach described in this paper placed this strain within the Coelastrella genus, therefore it was re-named to Coelastrella vacuolata MACC-549. The strain was selected for de novo sequencing based on its potential value in biohydrogen production as revealed in earlier studies. This is the first thorough report and characterization for green algae from the Coelastrella genus. The whole genome annotation of Coelastrella vacuolata MACC-549 (including nuclear, chloroplast and mitochondrial genomes) shed light on interesting metabolic and sexual breeding features of this algae and served as a basis to taxonomically classify this strain

Comparative genomics reveals the origin of fungal hyphae and multicellularity

Hyphae represent a hallmark structure of multicellular fungi. The evolutionary origins of hyphae and of the underlying genes are, however, hardly known. By systematically analyzing 72 complete genomes, we here show that hyphae evolved early in fungal evolution probably via diverse genetic changes, including co-option and exaptation of ancient eukaryotic (e.g. phagocytosis-related) genes, the origin of new gene families, gene duplications and alterations of gene structure, among others. Contrary to most multicellular lineages, the origin of filamentous fungi did not correlate with expansions of kinases, receptors or adhesive proteins. Co-option was probably the dominant mechanism for recruiting genes for hypha morphogenesis, while gene duplication was apparently less prevalent, except in transcriptional regulators and cell wall - related genes. We identified 414 novel gene families that show correlated evolution with hyphae and that may have contributed to its evolution. Our results suggest that hyphae represent a unique multicellular organization that evolved by limited fungal-specific innovations and gene duplication but pervasive co-option and modification of ancient eukaryotic functions

Gene age shapes the transcriptional landscape of sexual morphogenesis in mushroom forming fungi (Agaricomycetes)

Multicellularity has been one of the most important innovations in the history of life. The role of regulatory evolution in driving transitions to multicellularity is being increasingly recognized; however, patterns and drivers of transcriptome evolution are poorly known in many clades. We here reveal that allele-specific expression, natural antisense transcripts and developmental gene expression, but not RNA editing or a developmental hourglass act in concert to shape the transcriptome of complex multicellular fruiting bodies of fungi. We find that transcriptional patterns of genes are strongly predicted by their evolutionary age. Young genes showed more expression variation both in time and space, possibly because of weaker evolutionary constraint, calling for partially non-adaptive interpretations of evolutionary changes in the transcriptome of multicellular fungi. Gene age also correlated with function, allowing us to separate fruiting body gene expression related to simple sexual development from that potentially underlying complex morphogenesis. Our study highlighted a transcriptional complexity that provides multiple speeds for transcriptome evolution, but also that constraints associated with gene age shape transcriptomic patterns during transitions to complex multicellularity in fungi.Competing Interest StatementThe authors have declared no competing interest

Megaphylogeny resolves global patterns of mushroom evolution

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Megaphylogeny resolves global patterns of mushroom evolution

Mushroom-forming fungi (Agaricomycetes) have the greatest morphological diversity and complexity of any group of fungi. They have radiated into most niches and fulfil diverse roles in the ecosystem, including wood decomposers, pathogens or mycorrhizal mutualists. Despite the importance of mushroom-forming fungi, large-scale patterns of their evolutionary history are poorly known, in part due to the lack of a comprehensive and dated molecular phylogeny. Here, using multigene and genome-based data, we assemble a 5,284-species phylogenetic tree and infer ages and broad patterns of speciation/extinction and morphological innovation in mushroom-forming fungi. Agaricomycetes started a rapid class-wide radiation in the Jurassic, coinciding with the spread of (sub)tropical coniferous forests and a warming climate. A possible mass extinction, several clade-specific adaptive radiations and morphological diversification of fruiting bodies followed during the Cretaceous and the Paleogene, convergently giving rise to the classic toadstool morphology, with a cap, stalk and gills (pileate-stipitate morphology). This morphology is associated with increased rates of lineage diversification, suggesting it represents a key innovation in the evolution of mushroom-forming fungi. The increase in mushroom diversity started during the Mesozoic-Cenozoic radiation event, an era of humid climate when terrestrial communities dominated by gymnosperms and reptiles were also expanding.Fil: Varga, Torda. Hungarian Academy Of Sciences; HungríaFil: Krizsán, Krisztina. Hungarian Academy Of Sciences; HungríaFil: Földi, Csenge. Hungarian Academy Of Sciences; HungríaFil: Dima, Bálint. Eötvös Loránd University; HungríaFil: Sánchez-García, Marisol. Clark University; Estados UnidosFil: Lechner, Bernardo Ernesto. 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; ArgentinaFil: Sánchez-Ramírez, Santiago. University of Toronto; CanadáFil: Szöllosi, Gergely J.. Eötvös Loránd University; HungríaFil: Szarkándi, János G.. University Of Szeged; HungríaFil: Papp, Viktor. Szent István University; HungríaFil: Albert, László. Hungarian Mycological Society; HungríaFil: Andreopoulos, William. United States Department Of Energy. Joint Genome Institute; Estados UnidosFil: Angelini, Claudio. Jardin Botanico Nacional Ma. Moscoso; República DominicanaFil: Antonín, Vladimír. Moravian Museum; República ChecaFil: Barry, Kerrie W.. United States Department Of Energy. Joint Genome Institute; Estados UnidosFil: Bougher, Neale L.. Western Australian Herbarium; AustraliaFil: Buchanan, Peter. Manaaki Whenua-landcare Research; Nueva ZelandaFil: Buyck, Bart. Muséum National d'Histoire Naturelle; FranciaFil: Bense, Viktória. Hungarian Academy Of Sciences; HungríaFil: Catcheside, Pam. State Herbarium Of South Australia; AustraliaFil: Chovatia, Mansi. United States Department Of Energy. Joint Genome Institute; Estados UnidosFil: Cooper, Jerry. Manaaki Whenua-landcare Research; Nueva ZelandaFil: Dämon, Wolfgang. Oberfeldstrasse 9; AustriaFil: Desjardin, Dennis. San Francisco State University; Estados UnidosFil: Finy, Péter. Zsombolyai U. 56.; HungríaFil: Geml, József. Naturalis Biodiversity Center; Países BajosFil: Haridas, Sajeet. United States Department Of Energy. Joint Genome Institute; Estados UnidosFil: Hughes, Karen. University of Tennessee; Estados UnidosFil: Justo, Alfredo. Clark University; Estados UnidosFil: Karasinski, Dariusz. Polish Academy of Sciences; Poloni