Haploid Genome Analysis Reveals a Tandem Cluster of Four HSP20 Genes Involved in the High-Temperature Adaptation of Coriolopsis trogii.

Lining Wang,Shuiming Xiao,Zhihai Huang,Lu Gong,Baosheng Liao,Giuseppe Ianiri

doi:10.1128/spectrum.00287-21

Abstract

ABSTRACTCoriolopsis trogii is a typical thermotolerant basidiomycete fungus, but its thermotolerance mechanisms are currently unknown. In this study, two monokaryons of C. trogii strain Ct001 were assembled: Ct001_29 had a genome assembly size of 38.85 Mb and encoded 13,113 genes, while Ct001_31 was 40.19 Mb in length and encoded 13,309 genes. Comparative intra- and interstrain genomic analysis revealed the rich genetic diversity of C. trogii, which included more than 315,194 single-nucleotide polymorphisms (SNPs), 30,387 insertion/deletions (indels), and 1,460 structural variations. Gene family analysis showed that the expanded families of C. trogii were functionally enriched in lignocellulose degradation activities. Furthermore, a total of 14 allelic pairs of heat shock protein 20 (HSP20) genes were identified in the C. trogii genome. The expression profile obtained from RNA sequencing (RNA-Seq) showed that four tandem-duplicated allelic pairs, HSP20.5 to HSP20.8, had more than 5-fold higher expression at 35°C than at 25°C. In particular, HSP20.5 and HSP20.8 were the most highly expressed HSP20 genes. Allelic expression bias was found for HSP20.5 and HSP20.8; the expression of Ct29HSP20.8 was at least 1.34-fold higher than that of Ct31HSP20.8, and that of Ct31HSP20.5 was at least 1.5-fold higher than that of Ct29HSP20.5. The unique structural and expression profiles of the HSP20 genes revealed by these haplotype-resolved genomes provide insight into the molecular mechanisms of high-temperature adaptation in C. trogii.IMPORTANCE Heat stress is one of the most frequently encountered environmental stresses for most mushroom-forming fungi. Currently available fungal genomes are mostly haploid because high heterozygosity hinders diploid genome assembly. Here, two haplotype genomes of C. trogii, a thermotolerant basidiomycete, were assembled separately. A conserved tandem cluster of four HSP20 genes showing allele-specific expression was found to be closely related to high-temperature adaptation in C. trogii. The obtained haploid genomes and their comparison offer a more thorough understanding of the genetic background of C. trogii. In addition, the responses of HSP20 genes at 35°C, which may contribute to the growth and survival of C. trogii at high temperatures, could inform the selection and breeding of elite strains in the future.

Highlights

Coriolopsis trogii is a typical thermotolerant basidiomycete fungus, but its thermotolerance mechanisms are currently unknown
Heat shock protein 20 (HSP20) genes, which encode a fascinating group of molecular chaperones and comprise a major family of HSP genes, possess a conserved sequence of 80 to 100 amino acid residues, called an a-crystallin domain (ACD), in their C-terminal region [12]
The high degree of completeness of these assemblies was supported by the k-mer spectrum and by Benchmarking Universal Single-Copy Ortholog (BUSCO) analysis

Summary

Introduction

Coriolopsis trogii is a typical thermotolerant basidiomycete fungus, but its thermotolerance mechanisms are currently unknown. To investigate the molecular mechanisms of high-temperature adaptation in C. trogii, RNA-Seq analysis of mycelia cultured on different carbon sources and different temperatures, as well as during the different developmental stages of Ct001, was conducted (Fig. 4A and B).

Results

Conclusion