Telomere-to-telomere assembled and centromere annotated genomes of the two main subspecies of the button mushroom Agaricus bisporus reveal especially polymorphic chromosome ends

Abstract

Agaricus bisporus, the most cultivated edible mushroom worldwide, is represented mainly by the subspecies var. bisporus and var. burnettii. var. bisporus has a secondarily homothallic life cycle with recombination restricted to chromosome ends, while var. burnettii is heterothallic with recombination seemingly equally distributed over the chromosomes. to better understand the relationship between genomic make-up and different lifestyles, we have de novo sequenced a burnettii homokaryon and synchronised gene annotations with updated versions of the published genomes of var. bisporus. the genomes were assembled into telomere-to-telomere chromosomes and a consistent set of gene predictions was generated. the genomes of both subspecies were largely co-linear, and especially the chromosome ends differed in gene model content between the two subspecies. A single large cluster of repeats was found on each chromosome at the same respective position in all strains, harbouring nearly 50% of all repeats and likely representing centromeres. Repeats were all heavily methylated. finally, a mapping population of var. burnettii confirmed an even distribution of crossovers in meiosis, contrasting the recombination landscape of var. bisporus. The new findings using the exceptionally complete and well annotated genomes of this basidiomycete demonstrate the importance for unravelling genetic components underlying the different life cycles. The last decade has shown a sharp increase in the number of sequenced fungal genomes. Recently, the genome sequence of 90 mushrooms has been published 1 , but especially the ongoing 1,000 Fungal Genomes Project (https ://1000.funga lgeno mes.org/home/) will generate an extensive insight into the genomes of a wide range of fungal families and species. However, most genome sequences typify only one strain of a species, do not represent telomere-to-telomere chromosomes, do not have an accurate annotation of transposable elements, and centromeres remain unidentified. Especially complete and well annotated genomes of subspecies, with different life cycles, are a prerequisite to study the relation between genomic content and effects on different life cycles. A good example of a species with different life cycles is the button mushroom Agaricus bisporus, one of the most cultivated edible mushrooms in the world. It is an amphithallic basidiomycete represented mainly by two subspecies, i.e., Agaricus bisporus var. bisporus and A. bisporus var. burnettii. All commercial varieties

Mating-Type Locus Organization and Mating-Type Chromosome Differentiation in the Bipolar Edible Button Mushroom Agaricus bisporus

“…The two genomes of A. bisporus var. burnetti analysed, H119p1 and H119p4, are the two constituent homokaryons of opposite mating types isolated from the heterokaryon 119/9 (JB-13), originating from the Agaricus Recovery Program [ 31 ].…”

“…Short-read sequences of the genomes of the constituent homokaryons of the var. burnettii 119/9 strain (i.e., H119p1 and H119p4) [ 31 ] were assembled with SPAdes v3.11.1 [ 63 , 64 ] with a hybrid assembly approach by using the available PacBio genome of H119p4 [ 31 ] as a reference with the “--trusted-contigs” flag.…”

“…Furthermore, the non-sister segregation in meiosis, with recombination being restricted at the very edges of chromosomes in the studied cultivated strain of A. bisporus var. bisporus , ensures maintenance of heterozygosity across most loci [ 27 , 31 , 32 , 33 ]. While the formation of bi-spored basidia in the pseudo-homothallic A. bisporus var.…”

“…The four-spored heterothallic closely related variety A. bisporus var. burnettii , known from the Sonoran Desert of California [ 17 , 37 ], has on average 11 recombination events per individual per generation, evenly distributed along chromosomes [ 31 , 38 ]. As in the var.…”

Cycling in degradation of organic polymers and uptake of nutrients by a litter‐degrading fungus

“…Remaining reads were subjected to a second quality assessment using the FASTQC quality control tool version 0.11.5 (http://www.bioinformatics.babraham.ac.uk/projects/fastqc/) and deposited in NCBI GEO with accession number GSE124976. HISAT version 2.1.0 (Kim et al ., 2015) was used to align sequence reads to the Agabi_varbisH97_2 version of the A. bisporus H97 genome (Morin et al ., 2012; Sonnenberg et al ., 2020), which was obtained from MycoCosm (Grigoriev et al ., 2014). Cuffdiff (version 2.2.1), which is part of Cufflinks (Trapnell et al ., 2010), was used to identify reads mapping to predicted genes and to identify differentially expressed genes.…”