Auricularia heimuer is one of the most popular edible fungi in China. In this study, the whole genome of A. heimuer was sequenced on the Illumina HiSeq X system and compared with other mushrooms genomes. As a wood-rotting fungus, a total of 509 carbohydrate-active enzymes (CAZymes) were annotated in order to explore its potential capabilities on wood degradation. The glycoside hydrolases (GH) family genes in the A. heimuer genome were more abundant than the genes in the other 11 mushrooms genomes. The A. heimuer genome contained 102 genes encoding class III, IV, and V ethanol dehydrogenases. Evolutionary analysis based on 562 orthologous single-copy genes from 15 mushrooms showed that Auricularia formed an early independent branch of Agaricomycetes. The mating-type locus of A. heimuer was located on linkage group 8 by genetic linkage analysis. By combining the genome sequence analysis with the genetic linkage map, the mating-type locus of A. heimuer was located on scaffold45 and consisted of two subunits, α and β. Each subunit consisted of a pair of homeodomain mating-type protein genes HD1 and HD2. The mapping revealed conserved synteny at the whole mating-type loci and mirror symmetry relations near the β subunit between A. heimuer and Exidia glandulosa. This study proposed the potential for the bioethanol production by consolidated bioprocessing of A. heimuer. It will promote understanding of the lignocellulose degradation system and facilitate more efficient conversion of the agricultural wastes used for mushroom cultivation. It also will advance the research on the fruiting body development and evolution of A. heimuer.

Color is a crucial feature to consider when breeding and improving strains of Auricularia cornea. To uncover the mechanism of white strain formation in A. cornea, this study selected parental strains that were homozygous for the color trait and analyzed the genetic laws of A. cornea color through genetic population construction, such as test-cross, back-cross, and self-cross populations, and the statistical analysis of color trait segregation. Moreover, the study developed SSR molecular markers to construct a genetic linkage map, perform the fine mapping the color-controlling genetic locus, and verify candidate genes using yeast two-hybrid, transcriptome analysis, and different light treatments. The results of the study indicated that the color trait of A. cornea is controlled by two pairs of alleles. When both pairs of loci are dominant, the fruiting body is purple, while when both pairs of loci are recessive or one pair of loci is recessive, the fruiting body is white. Based on the linkage map, the study finely mapped the color locus within Contig9_29,619bp-53,463bp in the A. cornea genome and successfully predicted the color-controlling locus gene A18078 (AcveA), which belongs to the Velvet factor family protein and has a conserved structure domain of the VeA protein. It can form a dimer with the VelB protein to inhibit pigment synthesis in filamentous fungi. Lastly, the study validated the interaction between AcVeA and VelB (AcVelB) in A. cornea at the gene, protein, and phenotype levels, revealing the mechanism of inhibition of pigment synthesis in A. cornea. Under dark conditions, dimerization occurs, allowing it to enter the nucleus and inhibit pigment synthesis, leading to a lighter fruiting body color. However, under light conditions, the dimer content is low and cannot enter the nucleus to inhibit pigment synthesis. In summary, this study clarified the mechanism of white strain formation in A. cornea, which could aid in improving white strains of A. cornea and studying the genetic basis of color in other fungi.

Auricularia heimuer is drought tolerant, but the mechanism underlying its physiological response to drought has not been systematically studied. We selected 13 strains of A. heimuer and simulated drought stress using a complete yeast medium (CYM) containing 20% polyethylene glycol (PEG), while the medium used for the control treatments did not contain PEG. Strains were cultured on a shaker incubator at 25 °C at 120 rpm for 15 days under dark conditions. The contents of soluble sugars (SS) and soluble proteins (SP), the activities of superoxide dismutase (SOD) and catalase (CAT), the content of malondialdehyde (MDA), and the biomass were measured. Between the 20% PEG treatment and the control, as well as among different strains, there were significant differences in all of the physiological indices. The tested strains were classified into the following four categories according to their membership function values: the first category consisted of the highly drought-tolerant strain A; the second consisted of the drought-tolerant strains A127 and C; the third consisted of the moderately drought-tolerant strains A124, A14, A386, A462, A184, A496, A125, and B; and the fourth consisted of the drought-sensitive strains A356 and A508. Transcriptome analysis was performed on C before and after drought stress treatment, and 1762 differentially expressed genes (DEGs) were obtained, including 798 up- and 964 down-regulated genes. Through KEGG enrichment analysis, it was found for the first time that the synthesis pathway for trehalose in A. heimuer is trehalose phosphate synthase–trehalose phosphate phosphatase (TPS-TPP), which is involved in the response of A. heimuer to drought stress. In addition, two key enzyme genes involved in trehalose synthesis, namely trehalose-6-phosphate synthase (AhTPS) and trehalose-6-phosphate phosphatase (AhTPP), were significantly up-regulated after drought stress. The trehalose content significantly increased in 11 strains after drought stress treatment. This study discovered, for the first time, that the synthesis pathway of trehalose is involved in the response of edible fungi to drought stress, thus providing a reference for the genetic improvement of A. heimuer and the selection of drought-tolerant strains, laying a theoretical foundation for the resistance breeding of other edible fungi.

Auricularia heimuer is a widely cultivated jelly mushroom. The fruiting bodies are categorized into cluster and chrysanthemum types. With changing consumer demands and the need to reduce bio-waste, the demand for clustered fruiting bodies is increasing. Therefore, gene mining for fruiting body types is a matter of urgency. We determined that the A. heimuer locus for fruiting body type was located at one end of the genetic linkage map. The locus was localized between the markers D23860 and D389 by increasing the density of the genetic linkage map. BlastN alignment showed that the marker SCL-18 was also located between D23860 and D389, and a total of 25 coding genes were annotated within this interval. Through parental transcriptome analysis and qRT-PCR verification, the locus g7219 was identified as the gene controlling the fruiting body type. A single-nucleotide substitution in the TATA box of g7219 was detected between the parents. By PCR amplification of the promoter region of g7219, the TATA-box sequences of the cluster- and chrysanthemum-type strains were found to be CATAAAA and TATAAAA, respectively. This study provides a foundation for the breeding of fruiting body types and strain improvement of A. heimuer.

Auricularia heimuer is among China’s most important edible mushrooms and is rich in gum. With the improvement of people’s quality of life, demand is increasing for high-quality and good-tasting food; thus, the texture of A. heimuer is the focus of increasing attention. In this study, we added extra markers to a previously constructed genetic linkage map to generate a high-density genetic linkage map of A. heimuer, resolved the attributes of substrate quality-related traits, and performed quantitative trait locus (QTL) localization. The original genetic linkage map was improved by adding two new linkage groups, merging seven linkage groups into three linkage groups, and increasing the average linkage distance and total linkage estimated length. We anchored the 142 scaffolds of the genome to the improved genetic linkage map. In total, 15 significant QTLs controlling four quality-related traits were detected. Gumminess and chewiness, and cohesiveness and resilience, were linked. Three genes controlled cohesiveness and resilience; one gene controlled gumminess and chewiness. In conclusion, this study lays the foundation for gene localization and chromosome assembly in A. heimuer, elucidation of the mechanism of substrate quality-related trait formation, and provides a basis for precision breeding of A. heimuer.