Regulation of cyclic peptide biosynthesis in a plant pathogenic fungus by a novel transcription factor

Pedley, Kerry F.; Walton, Jonathan D.

doi:10.1073/pnas.231491298

Cited by 57 publications

(37 citation statements)

References 52 publications

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“…2A, 3, 6, 7, and 8). TOXE is a transcription factor that is necessary for expression of all of the known TOX2 genes, i.e., HTS1, TOXA, TOXC, TOXD, TOXF, and TOXG (3,16,37). Therefore, if resistance and/or the ability to crossprotect are a part of TOX2, these processes might also be regulated by TOXE.…”

Section: Resultsmentioning

confidence: 99%

“…One possible protection mechanism is rapid efflux of HC-toxin out of the cytoplasm by the product of TOXA, a putative MFS drug transporter (38). TOXA is tightly linked to HTS1, which encodes the nonribosomal peptide synthetase involved in HC-toxin biosynthesis, and is coregulated with the other genes involved in HC-toxin biosynthesis (1,37). The inability to recover TOXA mutants of Tox2 ϩ isolates, combined with its genetic association with the other HC-toxin biosynthetic genes, suggests that TOXA is an essential gene when the fungus is making HCtoxin, and therefore has a role in self-protection (38).…”

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confidence: 99%

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Characterization of Inhibitor-Resistant Histone Deacetylase Activity in Plant-Pathogenic Fungi

et al. 2002

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HC-toxin, a cyclic peptide made by the filamentous fungus Cochliobolus carbonum, is an inhibitor of histone deacetylase (HDAC) from many organisms. It was shown earlier that the HDAC activity in crude extracts of C. carbonum is relatively insensitive to HC-toxin as well as to the chemically unrelated HDAC inhibitors trichostatin and D85, whereas the HDAC activity of Aspergillus nidulans is sensitive (G. Brosch et al., Biochemistry 40:12855-12863, 2001). Here we report that HC-toxin-resistant HDAC activity was present in other, but not all, plant-pathogenic Cochliobolus species but not in any of the saprophytic species tested. The HDAC activities of the fungi Alternaria brassicicola and Diheterospora chlamydosporia, which also make HDAC inhibitors, were resistant. The HDAC activities of all C. carbonum isolates tested, except one non-toxin-producing isolate, were resistant. In a cross between a sensitive isolate and a resistant isolate, resistance genetically cosegregated with HC-toxin production. When fractionated by anion-exchange chromatography, extracts of resistant and sensitive isolates and species had two peaks of HDAC activity, one that was fully HC-toxin resistant and a second that was larger and sensitive. The first peak was consistently smaller in extracts of sensitive fungi than in resistant fungi, but the difference appeared to be insufficiently large to explain the differential sensitivities of the crude extracts. Differences in mRNA expression levels of the four known HDAC genes of C. carbonum did not account for the observed differences in HDAC activity profiles. When mixed together, resistant extracts protected extracts of sensitive C. carbonum but did not protect other sensitive Cochlibolus species or Neurospora crassa. Production of this extrinsic protection factor was dependent on TOXE, the transcription factor that regulates the HC-toxin biosynthetic genes. The results suggest that C. carbonum has multiple mechanisms of self-protection against HC-toxin.

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Section: Resultsmentioning

confidence: 99%

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confidence: 99%

Characterization of Inhibitor-Resistant Histone Deacetylase Activity in Plant-Pathogenic Fungi

et al. 2002

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“…In Claviceps purpurea, the CREB-like transcription factor CPTF1 is involved in oxidative stress response, and deletion of CPTF1 leads to reduced virulence (Nathues et al, 2004). ToxE is a pathway-specific transcription factor essential for the expression of HC-toxin required for pathogenicity of Cochliobolus carbonum (Pedley and Walton, 2001). Finally, in M. grisea, Mst12, a Ste12 homologue, was found to be essential for penetration and invasive growth (Park et al, 2002).…”

Section: Discussionmentioning

confidence: 99%

Biz1, a Zinc Finger Protein Required for Plant Invasion byUstilago maydis, Regulates the Levels of a Mitotic Cyclin

et al. 2006

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Plant invasion by pathogenic fungi involves regulated growth and highly organized fungal morphological changes. For instance, when the smut fungus Ustilago maydis infects maize (Zea mays), its dikaryotic infective filament is cell cycle arrested, and appressoria are differentiated prior to plant penetration. Once the filament enters the plant, the cell cycle block is released and fungal cells begin proliferation, suggesting a tight interaction between plant invasion and the cell cycle and morphogenesis control systems. We describe a novel factor, Biz1 (b-dependent zinc finger protein), which has two Cys 2 His 2 zinc finger domains and nuclear localization, suggesting a transcriptional regulatory function. The deletion of biz1 shows no detectable phenotypic alterations during axenic growth. However, mutant cells show a severe reduction in appressoria formation and plant penetration, and those hyphae that invade the plant arrest their pathogenic development directly after plant penetration. biz1 is induced via the b-mating-type locus, the key control instance for pathogenic development. The gene is expressed at high levels throughout pathogenic development, which induces a G2 cell cycle arrest that is a direct consequence of the downregulation of the mitotic cyclin Clb1. Our data support a model in which Biz1 is involved in cell cycle arrest preceding plant penetration as well as in the induction of appressoria.

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“…Another example of a probable pathway-specific regulator is the TOXE transcription factor, which is essential for the production of HC toxin, a cyclic tetrapeptide, in plant-pathogenic strains of Cochliobolus carbonum (2). TOXE is the prototype of a new family of transcription factors and is characterized by a DNA-binding domain with a basic region and four ankyrin repeats (25).…”

Section: Discussionmentioning

confidence: 99%

Winged Helix Transcription Factor CPCR1 Is Involved in Regulation of β-Lactam Biosynthesis in the Fungus Acremonium chrysogenum

et al. 2004

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Winged helix transcription factors, including members of the forkhead and the RFX subclasses, are characteristic for the eukaryotic domains in animals and fungi but seem to be missing in plants. In this study, in vitro and in vivo approaches were used to determine the functional role of the RFX transcription factor CPCR1 from the filamentous fungus Acremonium chrysogenum in cephalosporin C biosynthesis. Gel retardation analyses were applied to identify new binding sites of the transcription factor in an intergenic promoter region of cephalosporin C biosynthesis genes. Here, we illustrate that CPCR1 recognizes and binds at least two sequences in the intergenic region between the pcbAB and pcbC genes. The in vivo relevance of the two sequences for gene activation was demonstrated by using pcbC promoter-lacZ fusions in A. chrysogenum. The deletion of both CPCR1 binding sites resulted in an extensive reduction of reporter gene activity in transgenic strains (to 12% of the activity level of the control). Furthermore, Acremonium transformants with multiple copies of the cpcR1 gene and knockout strains support the idea of CPCR1 being a regulator of cephalosporin C biosynthesis gene expression. Significant differences in pcbC gene transcript levels were obtained with the knockout transformants. More-than-twofold increases in the pcbC transcript level at 24 and 36 h of cultivation were followed by a reduction to approximately 80% from 48 to 96 h in the knockout strain. The overall levels of the production of cephalosporin C were identical in transformed and nontransformed strains; however, the knockout strains showed a striking reduction in the level of the biosynthesis of intermediate penicillin N to less than 20% of that of the recipient strain. We were able to show that the complementation of the cpcR1 gene in the knockout strains reverses pcbC transcript and penicillin N amounts to levels comparable to those in the control. These results clearly indicate the involvement of CPCR1 in the regulation of cephalosporin C biosynthesis. However, the complexity of the data points to a well-controlled or even functional redundant network of transcription factors, with CPCR1 being only one player within this process.

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Regulation of cyclic peptide biosynthesis in a plant pathogenic fungus by a novel transcription factor

Cited by 57 publications

References 52 publications

Characterization of Inhibitor-Resistant Histone Deacetylase Activity in Plant-Pathogenic Fungi

Characterization of Inhibitor-Resistant Histone Deacetylase Activity in Plant-Pathogenic Fungi

Biz1, a Zinc Finger Protein Required for Plant Invasion byUstilago maydis, Regulates the Levels of a Mitotic Cyclin

Winged Helix Transcription Factor CPCR1 Is Involved in Regulation of β-Lactam Biosynthesis in the Fungus Acremonium chrysogenum

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