The dikaryotic stage dominates most of the life cycle in basidiomycetes, and each cell carries two different haploid nuclei. Accurate phasing of these two nuclear genomes and their interactions have long been of interest.
Our study combined PacBio HiFi reads, Nanopore ultra-long reads as well as Hi-C data to generate a complete, high-quality asymmetric dikaryotic genome of Tremella fuciformis Tr01, including Haplotypes A and B genomes. A meiotic haploid DBZ04 genome was assembled to detect three recombination events these two haplotypes. Several chromosomal rearrangements were identified, resulted in chromosome number, length, content, and sequence arrangement differences between the two haplotypes. Each nucleus had a two-speed genome, harboring three accessory chromosomes and two accessory compartments that can affect horizontal chromatin transfer between nuclei. Few basidiospores were ejected from fruiting bodies of Tr01. Most monospore isolates sequenced belonged to Tr01-Haplotype A genome architecture. More than one-third of monospore isolates carried one or two extra chromosomes including Chr12B and two new chromosomes ChrN1 and ChrN2. We hypothesize that the homologous regions of seven sister chromatids paired into a large complex during meiosis, which was followed by inter-chromosomal recombination at physical contact sites and formation of new chromosomes.
Two haplotype genomes in T. fuciformis Tr01 were assembled, the first description of basidiomycetous genomes with discrete genomic architecture. Meiotic activities of the asymmetric dikaryotic genomes resulted in formation of new chromosomes, aneuploidy of some daughter cells and inviability of most other daughter cells. A new approach was proposed for sporeless mushroom breeding.