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Abstract Haplotype-resolved chromosomal reference genomes are increasingly available for many fungi, offering insights into the evolution of pathogenic and symbiotic lifestyles. However, these resources remain scarce for ectomycorrhizal fungi, which play crucial roles in forest ecosystems. Here, we used a combination of chromatin conformation capture and PacBio sequencing to construct a haplotype-resolved chromosomal genome assembly for Boletus edulis, a prized edible fungus and emerging model for ectomycorrhizal fungal research. Our new reference assembly, “BolEdBiel_h2,” derives from a B. edulis sporocarp sampled in Bielefeld, Germany. The genome assembly spans 41.8 Mb, with a scaffold N50 of 4.1 Mb, and includes 11 chromosome-level scaffolds, achieving near telomere-to-telomere coverage across multiple chromosomes. We annotated a total of 15,406 genes, with a Benchmarking Universal Single-Copy Orthologs score of 96.2%. Key genomic features such as mating loci, carbohydrate-active enzymes, and effector proteins, were identified. As a first application of this new genomic resource, we mapped whole-genome resequencing data from 53 genets to investigate the population structure and genetic diversity of the European lineage of B. edulis. We identified 2 distinct genetic clusters and found that high-latitude populations from Iceland and Fennoscandia exhibited greater nucleotide diversity than populations from the United Kingdom and Central Europe. Additionally, we discovered a 0.4-Mb inversion on chromosome 3 and identified several regions of locally elevated nucleotide diversity, which may represent candidates for ecological adaptation. This genomic resource will facilitate a deeper understanding of this ecologically and commercially important wild fungus. 

Abstract Inbreeding, the mating of individuals that are related through common ancestry, is of central importance in evolutionary and conservation biology due to its impacts on individual fitness and population dynamics. However, while advanced genomic approaches have revolutionised the study of inbreeding in animals, genomic studies of inbreeding are rare in plants and lacking in fungi. We investigated global patterns of inbreeding in the prized edible porcini mushroomBoletus edulisusing 225 whole genomes from seven lineages distributed across the northern hemisphere. Genomic inbreeding was quantified using runs of homozygosity (ROHs). We found appreciable variation both among and within lineages, with some individuals having over 20% of their genomes in ROHs. Much of this variation could be explained by a combination of elevation and latitude, and to a lesser extent by predicted habitat suitability during the last glacial maximum. In line with this, the majority of ROHs were short, reflecting ancient common ancestry dating back approximately 200–1700 generations ago, while longer ROHs indicative of recent common ancestry (less than approximately 50 generations ago) were infrequent. Our study reveals the inbreeding legacy of major climatic events in a widely distributed forest mutualist, aligning with prevailing theories and empirical studies of the impacts of historical glaciation events on the dominant forest tree species of the northern hemisphere. 

Psychoactive mushrooms in the genusPsilocybehave immense cultural value and have been used for centuries in Mesoamerica. Despite the recent surge of interest in these mushrooms due to the psychotherapeutic potential of their natural alkaloid psilocybin, their phylogeny and taxonomy remain substantially incomplete. Moreover, the recent elucidation of the psilocybin biosynthetic gene cluster is known for only five of ~165 species ofPsilocybe, four of which belong to only one of two major clades. We set out to improve the phylogeny ofPsilocybeusing shotgun sequencing of fungarium specimens, from which we obtained 71 metagenomes including from 23 types, and conducting phylogenomic analysis of 2,983 single-copy gene families to generate a fully supported phylogeny. Molecular clock analysis suggests the stem lineage ofPsilocybearose ~67 mya and diversified ~56 mya. We also show that psilocybin biosynthesis first arose inPsilocybe, with 4 to 5 possible horizontal transfers to other mushrooms between 40 and 9 mya. Moreover, predicted orthologs of the psilocybin biosynthetic genes revealed two distinct gene orders within the biosynthetic gene cluster that corresponds to a deep split within the genus, possibly a signature of two independent acquisitions of the cluster withinPsilocybe.