Transcription in fungal conidia before dormancy produces phenotypically variable conidia that maximize survival in different environments

Chromatin immunoprecipitation followed by sequencing and RNA sequencing analyses reveal that the transcriptional activity of fungal conidia (spores) before dormancy contributes to conidia maturation and impacts fitness, drug resistance and virulence following germination. Fungi produce millions of clonal asexual conidia (spores) that remain dormant until favourable conditions occur. Conidia contain abundant stable messenger RNAs but the mechanisms underlying the production of these transcripts and their composition and functions are unknown. Here, we report that the conidia of three filamentous fungal species (Aspergillus nidulans, Aspergillus fumigatus, Talaromyces marneffei) are transcriptionally active and can synthesize mRNAs. We find that transcription in fully developed conidia is modulated in response to changes in the environment until conidia leave the developmental structure. Environment-specific transcriptional responses can alter conidial content (mRNAs, proteins and secondary metabolites) and change gene expression when dormancy is broken. Conidial transcription affects the fitness and capabilities of fungal cells after germination, including stress and antifungal drug (azole) resistance, mycotoxin and secondary metabolite production and virulence. The transcriptional variation that we characterize in fungal conidia explains how genetically identical conidia mature into phenotypically variable conidia. We find that fungal conidia prepare for the future by synthesizing and storing transcripts according to environmental conditions present before dormancy.

Automated summary

Transcriptional activity of fungal conidia before dormancy plays a crucial role in conidia maturation, fitness, drug resistance, and virulence post-germination. The environmental-specific transcriptional responses can alter conidial content and gene expression, affecting the capabilities of fungal cells after germination. Fungal conidia prepare for the future by synthesizing and storing transcripts according to environmental conditions present before dormancy.