The First Whole Genome Sequencing of Sanghuangporus sanghuang Provides Insights into Its Medicinal Application and Evolution

Abstract

Sanghuangporus is a medicinal macrofungal genus typified by S. sanghuang, the very species utilized in traditional Chinese medicines by Chinese ancient people. To facilitate the medicinal application of S. sanghuang, we, for the first time, perform its genome sequencing and analyses from a monokaryon strain. A 33.34 Mb genome sequence was assembled to 26 contigs, which lead to the prediction of 8278 protein-coding genes. From these genes, the potential biosynthesis pathway of sesquiterpenoids was, for the first time, identified from Sanghuangporus, besides that of triterpenoids. While polysaccharides are the main medicinal metabolites in S. sanghuang, flavonoids are especially abundant medicinal metabolites comparing with other medicinal macrofungal groups. From the genomic perspective, S. sanghuang has a tetrapolar heterothallic mating system, and has its special nutritional strategy and advantageous medicinal properties compared with S. baumii and S. vaninii. A phylogenomics analysis indicates that Sanghuangporus emerged 15.39 million years ago and S. sanghuang has a closer phylogenetic relationship with S. baumii than S. vaninii. However, S. sanghuang shares a higher region of synteny and more orthologous genes, including carbohydrate-active enzymes with S. vaninii than S. baumii. A comparative genomics analysis with S. baumii and S. vaninii indicates that species diversification within Sanghuangporus may be driven by the translocation and translocation plus inversion of genome sequences, while the expansion and contraction of gene families may contribute to the host specificity of Sanghuangporus species. In general, the genome sequence of S. sanghuang provides insights into its medicinal application and evolution.

Keywords: Basidiomycota; mating system; secondary metabolites; species diversification; wood-inhabiting macrofungi.

Figure 1

Characteristics of the de novo assembly genomic features of Sanghuangporus sanghuang. From the outside to the inside are: 1. Contigs (>1 Mb in length); 2. GC content: calculated as the percentage of G + C in 1 kb non-overlapping windows. The inward blue part represents the GC content in the region lower than the average genome GC content, while the outward purple part represents the opposite; 3. GC skew: calculated as the percentage of (G − C)/(G + C) in 1 kb non-overlapping windows. The inward green part represents G/C < 1, while the outward pink part represents G/C > 1; 4. Gene density: four circles starting from the orange color to inside, respectively, represent the numbers of coding genes, rRNA, snRNA and tRNA in 1 kb non-overlapping windows. The intensity of the color positively correlates with gene density; 5. Genome duplication: regions sharing more than 90% sequence similarity over 8 kb are connected by purple lines.

Figure 2

(A). Maximum clade credibility tree inferred from 429 single-copy orthologous genes. All nodes received full bootstrap support. The divergence time is labeled as the mean crown age for each node, while the 95% highest posterior density is also given within the Sanghuangporus clade. The numbers of gene family expansion and contraction in each species are labeled after plus (in red color) and minus (in green color) symbols, respectively. (B). Venn diagram of orthologous groups in Sanghuangporus baumii, S. sanghuang and S. vaninii.

Figure 3

Genomic synteny of Sanghuangporus baumii, S. sanghuang and S. vaninii. Shared blocks of synteny are linked by red lines between S. baumii and S. vaninii (62.77% syntenic genes in 95 blocks), green lines between S. baumii and S. sanghuang (65.51% syntenic genes in 96 blocks), and blue lines between S. sanghuang and S. vaninii (85.04% syntenic genes in 57 blocks).

Figure 4

Heatmap of CAZyme families found in Sanghuangporus baumii, S. sanghuang and S. vaninii. The x and y axes represent species and CAZyme families, respectively. Boxes are colored by the log values of gene numbers encoding CAZyme families. The box color from dark blue to dark red indicates the increase in gene numbers encoding CAZyme families.