Transcription Factors in the Fungus Aspergillus nidulans: Markers of Genetic Innovation, Network Rewiring and Conflict between Genomics and Transcriptomics

Gene regulatory networks (GRNs) are shaped by the democratic/hierarchical relationships among transcription factors (TFs) and associated proteins, together with the cis-regulatory sequences (CRSs) bound by these TFs at target promoters. GRNs control all cellular processes, including metabolism, stress response, growth and development. Due to the ability to modify morphogenetic and developmental patterns, there is the consensus view that the reorganization of GRNs is a driving force of species evolution and differentiation. GRNs are rewired through events including the duplication of TF-coding genes, their divergent sequence evolution and the gain/loss/modification of CRSs. Fungi (mainly Saccharomycotina) have served as a reference kingdom for the study of GRN evolution. Here, I studied the genes predicted to encode TFs in the fungus Aspergillus nidulans (Pezizomycotina). The analysis of the expansion of different families of TFs suggests that the duplication of TFs impacts the species level, and that the expansion in Zn2Cys6 TFs is mainly due to dispersed duplication events. Comparison of genomic annotation and transcriptomic data suggest that a significant percentage of genes should be re-annotated, while many others remain silent. Finally, a new regulator of growth and development is identified and characterized. Overall, this study establishes a novel theoretical framework in synthetic biology, as the overexpression of silent TF forms would provide additional tools to assess how GRNs are rewired.