Transcriptome data reveal conserved patterns of fruiting body development and response to heat stress in the mushroom-forming fungus Flammulina filiformis.

Xiao-Bin Liu,Yang-Yang Cui,Jing Li,Pan-Meng Wang,László G Nagy,Jin-Xia Zhang,Jian-Ping Xu,Zhu L Yang,Bao-Gui Xie,Meng Li,Jun-Jie Yan,En-Hua Xia,Katherine A Borkovich

doi:10.1371/journal.pone.0239890

Abstract

Mushroom-forming fungi are complex multicellular organisms that form the basis of a large industry, yet, our understanding of the mechanisms of mushroom development and its responses to various stresses remains limited. The winter mushroom (Flammulina filiformis) is cultivated at a large commercial scale in East Asia and is a species with a preference for low temperatures. This study investigated fruiting body development in F. filiformis by comparing transcriptomes of 4 developmental stages, and compared the developmental genes to a 200-genome dataset to identify conserved genes involved in fruiting body development, and examined the response of heat sensitive and -resistant strains to heat stress. Our data revealed widely conserved genes involved in primordium development of F. filiformis, many of which originated before the emergence of the Agaricomycetes, indicating co-option for complex multicellularity during evolution. We also revealed several notable fruiting-specific genes, including the genes with conserved stipe-specific expression patterns and the others which related to sexual development, water absorption, basidium formation and sporulation, among others. Comparative analysis revealed that heat stress induced more genes in the heat resistant strain (M1) than in the heat sensitive one (XR). Of particular importance are the hsp70, hsp90 and fes1 genes, which may facilitate the adjustment to heat stress in the early stages of fruiting body development. These data highlighted novel genes involved in complex multicellular development in fungi and aid further studies on gene function and efforts to improve the productivity and heat tolerance in mushroom-forming fungi.

Highlights

Mushroom-forming fungi are widely distributed through Earth’s ecosystems
These genes showed expression patterns similar to those in the RNAseq data (S1 Fig), indicating that our transcriptome sequencing provided a good estimate of gene expression patterns in the analyses of fruiting body development and heat stress response of F. filiformis
This study broadened our knowledge of fruiting body development and heat stress response of mushroom-forming fungi based on comparisons of transcriptomic data in F. filiformis

Summary

Introduction

Mushroom-forming fungi are widely distributed through Earth’s ecosystems. They play essential roles in nutrient cycling, environmental protection, plant and animal health [1,2,3]. Studies focused on ecologically or economically important non-model species, which included the saprotrophic fungi (Agaricus bisporus, Flammulina filiformis, Lentinula edodes, Lentinus tigrinus, Cyclocybe aegerita), plant pathogen (Armillaria ostoyae), and the ectomycorrhizal fungi (Laccaria bicolor) [2, 19,20,21,22,23,24,25,26] These studies broadened our knowledge on fruiting body development and highlighted conserved expression patterns of some key developmental genes (such as the genes encoding light receptors (white collar complex), transcription factors (c2h2, hom, hom2), CAZyme and F-box protein etc.), indicating conserved molecular mechanisms in multicellular complexity in Agaricomycetes. Mushroom development is a highly organized process, and genetic drivers of spatial and temporal differentiation events are not known, and our understanding of mushroom formation in other ecologically and economically important mushroom-forming fungi is still in its infancy [12, 13, 27, 28]

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