Transcription factor lineages in plant-pathogenic fungi, connecting diversity with fungal virulence

Abstract

Plant-pathogenic fungi span diverse taxonomic lineages. Their host-infection strategies are often specialised and require the coordinated regulation of molecular virulence factors. Transcription factors (TFs) are fundamental regulators of gene expression, controlling development and virulence in plant pathogenic fungi. Recent research has established regulatory roles for several taxonomically conserved fungal TFs, but the evolution of specific virulence regulators is not well understood. This study sought to explore the representation of TFs across a taxonomically-diverse range of fungi, with a focus on plant pathogens. A significant trend was observed among the obligate, host-associated pathogens, which possess a reduced overall TF repertoire, alluding to a lack of pressure for maintaining diversity. A novel orthology-based analysis is then presented that refined TF classifications, traditionally based on the nature of the DNA-binding domains. Using this analysis, cases of TF over/underrepresentation across fungal pathogen lineages are systematically highlighted. Specific examples are then explored and discussed that included the TF orthologues of Ste12, Pf2 and EBR1, plus phytotoxic secondary-metabolite cluster regulators, which all presented novel and distinct evolutionary insights. Ultimately, as the examples presented demonstrate, this resource can be interrogated to guide functional studies that seek to characterise virulence-specific regulators and shed light on the factors underpinning plant pathogenicity.

Chromatin-immunoprecipitation reveals the PnPf2 transcriptional network controlling effector-mediated virulence in a fungal pathogen of wheat

“…A ‘fungal TF domain’ was identified from a.a 223 to 294 within a conserved ‘middle homology region’ (a.a 104 to 320). These features are frequently observed in Zn 2 Cys 6 TFs and have been linked to the modulation of TF activity (26, 27, 15). A structurally disordered domain, typically associated with post-translational modifications and intermolecular interactions (28), was also identified at the C-terminus of PnPf2.…”

“…Two additional TF-encoding genes were simultaneously investigated. This included SNOG_08565, identified in the PnPf2 lineage of fungal TFs (15) suggesting a possible common evolutionary origin. It also included SNOG_03067 ( PnEbr1 ), which is co-expressed with PnPf2, ToxA , Tox1 and Tox3 high during early infection ( Fig.…”

“…Therefore, some shared regulatory pathways likely exist with Pf2 orthologues given the evidence for at least one conserved binding mechanism. However, there are major a.a polymorphisms between AmyR and Pf2 orthologues at the Zn 2 Cys 6 DNA-binding domain (15) and M1 has not been reported as an AmyR target despite extensive motif investigation (38, 32). It is therefore conceivable that M1 is a regulatory binding element unique to Pf2 orthologues and therefore useful to identify putative direct targets such as ToxA in P. nodorum .…”

“…The Pf2 orthologues can be traced across several Ascomycota fungal lineages that include the Dothideomycetes, Leotiomycetes and Soradiomycetes (15). Genedeletion in the plant pathogens Botrytis cinerea, Fusarium spp., Magnaporthe oryzae…”

“…The Pf2 orthologues can be traced across several Ascomycota fungal lineages that include the Dothideomycetes, Leotiomycetes and Soradiomycetes (15). Gene-deletion in the plant pathogens Botrytis cinerea , Fusarium spp., Magnaporthe oryzae and Zymoseptoria tritici all suppressed fungal virulence as well as their capacity to utilise alternative carbon sources (16–19).…”