Rewiring of transcriptional networks as a major event leading to the diversity of asexual multicellularity in fungi

Abstract

Complex multicellularity (CM) is characterized by the generation of threedimensional structures that follow a genetically controlled program. CM emerged at least five times in evolution, one of them in fungi. There are two types of CM programs in fungi, leading, respectively, to the formation of sexual or asexual spores. Asexual spores foment the spread of mycoses, as they are the main vehicle for dispersion. In spite of this key dependence, there is great morphological diversity of asexual multicellular structures in fungi. To advance the understanding of the mechanisms that control initiation and progression of asexual CM and how they can lead to such a remarkable morphological diversification, we compiled 500 fungal proteomes, representing all phyla and subphyla, and most known classes. Conservation analyses of 32 regulators of asexual development suggest stepwise emergence of transcription factors. While velvet proteins constitute one of the most ancient systems, the central regulator BrlA emerged late in evolution (with the class eurotiomycetes). Some factors, such as MoConX4, seem to be species-specific. These observations suggest that the emergence and evolution of transcriptional regulators rewire pre-existing transcriptional networks. This process could reach the species level, resulting in a vast diversity of morphologies.

Defining the transcriptional responses of Aspergillus nidulans to cation/alkaline pH stress and the role of the transcription factor SltA

“…Future work will focus on delimiting the role of SltA on the ambient pH regulatory pathway and whether corregulation with PacX/An0766 occurs, since both SltA and PacX are transcription factors specific to the subphylum Pezizomycotina [5,23,43]. In the context of ancient gene rewiring phenomena [66], both factors may have been recruited for new functions in ancestors of Aspergillus species. Deciphering the roles of SltA in distant Pezizomycotina species would contribute to our understanding these genetic processes and dissection of the mechanisms of abiotic stress response in fungi.…”

A 21st century miniguide to sporophore morphogenesis and development in Agaricomycetes and their biotechnological potential

“…These velvet regulators are present in most clades of the fungal kingdom from chytrids to basidiomycetes. Velvet proteins have presumably been recruited into the basidiome transcriptional circuit as they are one of the most ancient systems regulating the production of asexual spores in fungi (Etxebeste et al, 2019). In contrast to the central regulator BrlA, which regulates Aspergillus conidiophores and emerged later in fungal evolution, with the class Eurotiomycetes.…”

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

“…1999 ), and budding yeasts ( Sorrells and Johnson 2015 ; Nocedal et al. 2017 ), we still know little about how the evolution of developmental GRNs is associated with the wide range of morphological diversity in the fungal kingdom ( Etxebeste et al. 2019 ).…”