Developmental transcriptomics of Chinese cordyceps reveals gene regulatory network and expression profiles of sexual development-related genes

Abstract

Background Chinese cordyceps, also known as Chinese caterpillar fungus ( Ophiocordyceps sinensis , syn. Cordyceps sinensis ), is of particular interest for its cryptic life cycle and economic and ecological importance. The large-scale artificial cultivation was succeeded recently after several decades of efforts and attempts. However, the induction of primordium, sexual development of O. sinensis and the molecular basis of its lifestyle still remain cryptic. Results The developmental transcriptomes were analyzed for six stages covering the whole developmental process, including hyphae (HY), sclerotium (ST), primordium (PR), young fruiting body (YF), developed fruiting body (DF) and mature fruiting body (MF), with a focus on the expression of sexual development-related genes. Principal component analysis revealed that the gene expression profiles at the stages of primordium formation and fruiting body development are more similar than those of the undifferentiated HY stage. The PR and MF stages grouped together, suggesting that primordium differentiation and sexual maturation have similar expression patterns. Many more DEGs were identified between the ST and HY stages, covering 47.5% of the O. sinensis genome, followed by the comparisons between the ST and PR stages. Using pairwise comparisons and weighted gene coexpression network analysis, modules of coexpressed genes and candidate hub genes for each developmental stage were identified. The four mating type loci genes expressed during primordium differentiation and sexual maturation; however, spatiotemporal specificity of gene expression indicated that they also expressed during the anamorphic HY stage. The four mating type genes were not coordinately expressed, suggesting they may have divergent roles. The expression of the four mating type genes was highest in the fertile part and lowest in the sclerotium of the MF stage, indicating that there is tissue specificity. Half of genes related to mating signaling showed as the highest expression in the ST stage, indicating fruiting was initiated in the ST stage. Conclusions These results provide a new perspective to understanding of the key pathways and hub genes, and sexual development-related gene profile in the development of Chinese cordyceps. It will be helpful for underlying sexual reproduction, and add new information to existing models of fruiting body development in edible fungi. Electronic supplementary material The online version of this article (10.1186/s12864-019-5708-z) contains supplementary material, which is available to authorized users.

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“…In agreement with this, comparisons between the two adjacent stages for primordia and fruiting bodies had fewer differentially expressed genes, confirming the similar gene expression patterns between primordia and fruiting bodies. This is consistent with the gene expression profiles of O. sinensis at differential development stages [24] , [44] . In this study, a low level correlation was found between the transcriptomic and proteomic data ( Fig.…”

“…Because of its medicinal and nutritional values, O. sinensis has historically been regarded as the most valued traditional Chinese medicinal fungus. Recently, numerous transcriptomic, proteomic and metabolomic data have revealed fruiting body and sexual development-related genes [24] , the protein uniformity between wild and artificial fruiting bodies [25] and metabolite differences between O. sinensis and C. militaris [43] . Compared to O. sinensis , T. guangdongense contains similar metabolites and can be easily artificially cultivated [5] .…”

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“…Recently, transcriptome analyses have compared the transcripts of six O. sinensis developmental stages, and concluded that fungi in primordium differentiation and sexual maturation display similar gene expression patterns. Moreover, half of the genes related to mating showed the highest expression in the ST stage, indicating that fruiting in this fungus is initiated in the ST stage 12 . Previously, we compared transcript expression in three other stages of the fungal life cycle (asexual mycelium, developing fruiting body, and mature fruiting body).…”

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