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The formation of multicellular fruiting bodies in basidiomycete mushrooms is a crucial developmental process for sexual reproduction and subsequent spore development. Temperature is one of the most critical factors influencing the phase transition for mushroom reproduction. During the domestication of mushrooms, traits related to fruiting bodies have significantly impacted agricultural adaptation and human preferences. Recent research has demonstrated that chromosomal variations, such as structural variants (SVs) and variant blocks (VBs), play crucial roles in agronomic traits and evolutionary processes. However, the lack of high-quality genomic information and important trait data have hindered comprehensive identification and characterization in Lentinula edodes breeding processes. In this study, the genomes of two monokaryotic L. edodes strains, characterized by thermo-tolerance and thermo-sensitivity during fruiting body formation, were reassembled at the chromosomal level. Comparative genomic studies of four thermo-tolerant and thermo-sensitive monokaryotic L. edodes strains identified a 0.56 Mbp variant block on chromosome 9. Genes associated with DNA repair or cellular response to DNA damage stimulus were enriched in this variant block. Finally, we developed eight CAPS markers from the variant block to discriminate the thermo-tolerant traits in L. edodes cultivars. Our findings show that the identified variant block is highly correlated with the thermo-tolerant trait for fruiting body formation and that alleles present in this block may have been artificially selected during L. edodes domestication.

Lentinula edodes is a globally important edible mushroom species that is appreciated for its medicinal properties as well as its nutritional value. During commercial cultivation, a mycelial brown film forms on the surface of the sawdust growth medium at the late vegetative stage. Mycelial film formation is a critical developmental process that contributes to the quantity and quality of the mushroom yield. However, little is known regarding the genetic underpinnings of brown film formation on the surface of mycelial tissue. A novel causal gene associated with the formation of the mycelial brown film, named ABL (Abnormal browning related to light), was identified in this study. The comparative genetic analysis by dihybrid crosses between normal and abnormal browning film cultivars demonstrated that a single dominant allele was responsible for the abnormal mycelium browning phenotype. Whole-genome sequencing analysis of hybrid isolates revealed five missense single-nucleotide polymorphisms (SNPs) in the ABL locus of individuals forming abnormal partial brown films. Additional whole-genome resequencing of a further 16 cultivars showed that three of the five missense SNPs were strongly associated with the abnormal browning phenotype. Overexpression of the dominant abl-D allele in a wild-type background conferred the abnormal mycelial browning phenotype upon transformants, with slender hyphae observed as a general defective mycelial growth phenotype. Our methodology will aid the future discovery of candidate genes associated with favorable traits in edible mushrooms. The discovery of a novel gene, ABL, associated with mycelial film formation will facilitate marker-associated breeding in L. edodes.