Tpc1 is an important Zn(II)2Cys6 transcriptional regulator required for polarized growth and virulence in the rice blast fungus.
Tpc1 is an important Zn(II)2Cys6 transcriptional regulator required for polarized growth and virulence in the rice blast fungus.
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DOI:
10.1371/journal.ppat.1006516
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发表时间:
2017-07
期刊:
影响因子:
6.7
通讯作者:
Sesma A
中科院分区:
文献类型:
--
作者:
Galhano R;Illana A;Ryder LS;Rodríguez-Romero J;Demuez M;Badaruddin M;Martinez-Rocha AL;Soanes DM;Studholme DJ;Talbot NJ;Sesma A
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. Cellular polarity is an intrinsic feature of filamentous fungal growth and pathogenesis. In this study, we identified a gene required for fungal polar growth and virulence in the rice blast fungus Magnaporthe oryzae. This gene has been named TPC1 (Transcription factor for Polarity Control 1). The Tpc1 protein belongs to the fungal Zn(II)2Cys6 binuclear cluster family. This DNA-binding motif is present exclusively in the fungal kingdom. We have characterised defects associated with lack of Tpc1 in M. oryzae. We show that Tpc1 is involved in polarised growth and virulence. The M. oryzae Δtpc1 mutant shows a delay in glycogen and lipid metabolism, and infection-associated autophagy–processes that regulate appressorium-mediated M. oryzae plant infection. The saprophytic fungus Neurospora crassa contains a Tpc1 homolog (NcTpc1) involved in vegetative growth and sustained tip elongation, suggesting that Tpc1-like proteins act as core regulators of polarised growth and development in filamentous fungi. A comparative transcriptome analysis has allowed us to identify genes regulated by Tpc1 in M. oryzae including NoxD, an important component of the fungal NADPH complex. Significantly, Tpc1 interacts with Mst12, a component of the Pmk1 signalling pathway essential for appressorium development, and modulates Mst12 binding affinity to NOXD promoter region. We conclude that Tpc1 is a key regulator of polarity in M. oryzae that regulates growth, autophagy and septin-mediated reorientation of the F-actin cytoskeleton to facilitate plant cell invasion.
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