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 studied 503 fungal proteomes, representing all phyla and subphyla, and most known classes. Conservation analyses of 33 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 transcriptional networks. This process could reach the species level, resulting in a vast diversity of morphologies.

Defining the transcriptional responses ofAspergillus nidulansto 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 occurs, since both SltA and PacX are transcription factors specific of Pezizomycotina subphylum [5, 20, 40]. In the context of ancient gene rewiring phenomena [62], 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 understand these genetic processes and dissect the mechanisms of abiotic stress response in fungi.…”

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

“…TFs and GRNs controlling in fungi, i.e., stress-response, carbon and nitrogen metabolism, light sensing and the induction/progression of developmental cycles were characterized for the first time in this Aspergillus species. Taking advantage of this knowledge, recent works have focused on the study of how some of these GRNs were structured during the evolution of the kingdom fungi (de Vries et al 2017;Ojeda-López et al 2018;Etxebeste et al 2019). An interesting feature of the TFomes of Ascomycota, in general, is the remarkable expansion of zinc cluster-type TFs, while in Basidiomycota and early diverging fungi, C2H2-type TFs are the most represented family (Shelest 2017).…”

“…Saccharomycetes have traditionally been used to study how GRNs are shaped and evolve (Nocedal and Johnson 2015;Sorrells and Johnson 2015;Britton et al 2020). Recent comparative studies carried out in Basidiomycetes and Ascomycetes have shown that TFs controlling (asexual and/or sexual) developmental patterns emerged gradually in evolution (Etxebeste et al 2019;Kiss et al 2019;Krizsán et al 2019). Furthermore, the formation of main clades such as that of Basidiomycota or that of the subphylum Pezizomycotina was accompanied by a boost in the number of TF-coding genes.…”

“…In the order Eurotiales, the transcription factor BrlA plays a role as a bottleneck in the formation of asexual structures known as conidiophores (Adams et al 1998). BrlA emerged much later than other upstream and downstream TFs of the same GRN (de Vries et al 2017;Ojeda-López et al 2018), suggesting that it caused rewiring events in pre-existent ancient networks (Etxebeste et al 2019).…”

The secondary metabolite regulator, BbSmr1, is a central regulator of conidiation via the BrlA‐AbaA‐WetA pathway in Beauveria bassiana

“…Similar to other filamentous fungi, conidiation of B. bassiana begins with a phenotypic change, the formation of conidiophores from aerial vegetative mycelium, which is followed by the production of conidia on conidiophores. Fungal conidiation processes are affected by many ambient factors, such as light, nutrients and stressors, and are temporally and spatially regulated by a discrete number of regulatory proteins, which are reviewed in previous articles (Park and Yu., 2012 and 2016; Rangel et al ., 2015; Etxebeste et al ., 2019; Ruger‐Herreros and Corrochano, 2020). The signal cascade BrlA‐AbaA‐WetA composes a conserved central developmental pathway (CDP) controlling conidial development in filamentous fungi and has been well clarified in the model fungus Aspergillus nidulans (Marshall and Timberlake, 1991; Andrianopoulos and Timberlake, 1994; Etxebeste et al ., 2010).…”