Tpc1 is an important Zn(II)2Cys6 transcriptional regulator required for polarized growth and virulence in the rice blast fungus

Abstract

The establishment of polarity is a critical process in pathogenic fungi, mediating infection-related morphogenesis and host tissue invasion. Here, we report the identification of TPC1 (Transcription factor for Polarity Control 1), which regulates invasive polarized growth in the rice blast fungus Magnaporthe oryzae. TPC1 encodes a putative transcription factor of the fungal Zn(II)2Cys6 family, exclusive to filamentous fungi. Tpc1-deficient mutants show severe defects in conidiogenesis, infection-associated autophagy, glycogen and lipid metabolism, and plant tissue colonisation. By tracking actin-binding proteins, septin-5 and autophagosome components, we show that Tpc1 regulates cytoskeletal dynamics and infection-associated autophagy during appressorium-mediated plant penetration. We found that Tpc1 interacts with Mst12 and modulates its DNA-binding activity, while Tpc1 nuclear localisation also depends on the MAP kinase Pmk1, consistent with the involvement of Tpc1 in this signalling pathway, which is critical for appressorium development. Importantly, Tpc1 directly regulates NOXD expression, the p22phox subunit of the fungal NADPH oxidase complex via an interaction with Mst12. Tpc1 therefore controls spatial and temporal regulation of cortical F-actin through regulation of the NADPH oxidase complex during appressorium re-polarisation. Consequently, Tpc1 is a core developmental regulator in filamentous fungi, linking the regulated synthesis of reactive oxygen species and the Pmk1 pathway, with polarity control during host invasion.

The Fungal-Specific Transcription Factor VpFSTF1 Is Required for Virulence in Valsa pyri

“…Moreover, these results indicate that VpFSTF1 is a multifunctional fungal-specific TF in V. pyri. The virulence reduction phenotype of the VpFSTF1 mutant is similar to the many reported Zn2Cys6 TFs mutants, including VdPf (Luo et al, 2016), AbPf2 (Cho et al, 2013), VdFTF1 (Zhang et al, 2017), TPC1 (Galhano et al, 2017), MoCOD1, and MoCOD2 (Chung et al, 2013). Similar but not the same, TPC1 can control the growth of mycelia (Galhano et al, 2017) while VdFTF1 has no impact on vegetative growth, mycelial pigmentation and conidial morphology (Zhang et al, 2017) and VdPf can influence conidial production and melanized microsclerotium formation (Luo et al, 2016).…”

The transcription factor Zt107320 affects the dimorphic switch, growth and virulence of the fungal wheat pathogen Zymoseptoria tritici

“…Similarly, a partial, but incomplete, reduction of invasive growth in planta is observed in ∆ MoCOD1 (Chung et al , ). The impact of Zt107320 on fungal growth and pathogenicity is similar to the effect caused by other members of the Zn(II) 2 Cys 6 transcription factor family: TPC1 regulates invasive, polarized growth and virulence in the rice blast fungus M. oryzae (Galhano et al , ), and the transcription factor FOW2 is known to control the ability of F. oxysporum to invade roots and colonize plant tissue (Imazaki et al , ).…”

“…This gene family of transcription factors is exclusive to fungi (MacPherson et al, 2006;Pan and Coleman, 1990) and many members play an important role in the regulation of fungal physiology. For example, Zn(II) 2 Cys 6 transcription factors in Magnaporthe oryzae, Fusarium oxysporum, Leptosphaeria maculans, Parastagonospora nodorum and Pyrenophora triticirepentis are involved in the regulation of fungal growth and pathogenicity (Fox et al, 2008;Galhano et al, 2017;Imazaki et al, 2007;Lu et al, 2014;Rybak et al, 2017). Interestingly, the homologue of Zt107320 in the rice blast pathogen M. oryzae, MoCOD1, was shown to affect conidiation and pathogenicity (Chung et al, 2013).…”

Virulence‐ and signaling‐associated genes display a preference for long 3′UTRs during rice infection and metabolic stress in the rice blast fungus

“…Fungal material was harvested from 60-h-old fungal mycelia grown in liquid CM, and then transferred for an additional 12 h into fresh liquid CM, MM, MM-N or MM-C. RNA was extracted using a LiCl protocol (Galhano et al, 2017). Three biological replicates were independently harvested and extracted for each library preparation.…”