Recurrent Loss of abaA, a Master Regulator of Asexual Development in Filamentous Fungi, Correlates with Changes in Genomic and Morphological Traits

Abstract

Gene regulatory networks (GRNs) drive developmental and cellular differentiation, and variation in their architectures gives rise to morphological diversity. Pioneering studies in Aspergillus fungi, coupled with subsequent work in other filamentous fungi, have shown that the GRN governed by the BrlA, AbaA, and WetA proteins controls the development of the asexual fruiting body, or conidiophore. A specific aspect of conidiophore development is the production of phialides, conidiophore structures that are under the developmental control of AbaA and function to repetitively generate spores. Fungal genome sequencing has revealed that some filamentous fungi lack abaA, and also produce asexual structures that lack phialides, raising the hypothesis that abaA loss is functionally linked to diversity in asexual fruiting body morphology. To examine this hypothesis, we carried out an extensive search for the abaA gene across 241 genomes of species from the fungal subphylum Pezizomycotina. We found that abaA was independently lost in four lineages of Eurotiomycetes, including from all sequenced species within the order Onygenales, and that all four lineages that have lost abaA also lack the ability to form phialides. Genetic restoration of abaA from Aspergillus nidulans into Histoplasma capsulatum, a pathogenic species from the order Onygenales that lacks an endogenous copy of abaA, did not alter Histoplasma conidiation morphology but resulted in a marked increase in spore viability. We also discovered that species lacking abaA contain fewer AbaA binding motifs in the regulatory regions of orthologs of some AbaA target genes, suggesting that the asexual fruiting body GRN of organisms that have lost abaA has likely been rewired. Our results provide an illustration of how repeated losses of a key regulatory transcription factor have contributed to the diversity of an iconic fungal morphological trait.

The PHD Transcription Factor Cti6 is Involved in the Fungal Colonization and Aflatioxin B1 Biological Synthesis of Aspergillus Flavus

“…However, there is no available report on the biological function of Cti6 in the filamentous fungi until now. (Sewall, 1994;Mead et al, 2020). By deletion of PHD and Atrophin-1 domain, it was found that, similar to Δcti6, the fungal colony size, mycelial density and conidiation state of PHD domain deletion strain (cti6 ΔPHD ) on both PDA media and crop kernels were significantly restrained compared to the Ctrl fungal strain, but Atrophin-1 domain was only involved in the sporulation of the fungus (Figure 2 and 5).…”

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

“…Knowledge gained can be extended to other fungal systems. Recently, new experimental approaches have been developed, focusing on the expression of genes encoding regulators of A. nidulans asexual reproduction with the aim of modifying developmental patterns of species such as Monascus ruber or Histoplasma capsulatum [12,86]. Although the trials were unable to trigger major morphological changes, they paved the way for the establishment of simple and reliable approaches for the experimental study of GRN rewiring and its consequences for organism evolution.…”

Transcription factors in the fungus Aspergillus nidulans: Markers of genetic innovation, network rewiring and conflict between genomics and transcriptomics

“…Knowledge thus gained can, of course, be extended to other fungal systems. Recently, new experimental approaches have been developed, focused on the expression of genes encoding regulators of A. nidulans asexual reproduction with the aim of modifying developmental patterns of species such as Monascus ruber or Histoplasma capsulatum [12, 88]. Although the trials were unable to trigger major morphological changes, they paved the way for the establishment of simple and reliable approaches for the experimental study of GRN rewiring and its consequences on organism evolution.…”