Transcription factor Rbf1 is the master regulator for b-mating type controlled pathogenic development in Ustilago maydis
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ABSTRACT:
ORGANISM(S): Mycosarcoma maydis
PROVIDER: GSE18881 | GEO | 2010/06/01
SECONDARY ACCESSION(S): PRJNA121275
REPOSITORIES: GEO
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Project description:In the phytopathogenic basidiomycete Ustilago maydis, sexual and pathogenic development are tightly connected and controlled by the heterodimeric bE/bW transcription factor complex encoded by the b-mating type locus. The formation of the active bE/bW heterodimer leads to the formation of filaments, induces a G2 cell cycle arrest, and triggers pathogenicity. Here, we identify a set of 345 bE/bW responsive genes which show altered expression during these developmental changes; several of these genes are associated with cell cycle coordination, morphogenesis and pathogenicity. 90% of the genes that show altered expression upon bE/bW-activation require the zinc finger transcription factor Rbf1, one of the few factors directly regulated by the bE/bW heterodimer. Rbf1 is a novel master regulator in a multilayered network of transcription factors that facilitates the complex regulatory traits of sexual and pathogenic development.
| S-EPMC2916880 | biostudies-literature
Project description:This SuperSeries is composed of the following subset Series: GSE18750: Controlled expression of compatible and incompatible combinations of Ustilago maydis b-mating type locus genes bE and bW GSE18754: Effect of rbf1 deletion during controlled expression of of Ustilago maydis b-mating type locus genes bE1 and bW2 GSE18756: Rbf1 induced gene expression in Ustilago maydis Refer to individual Series
2010-06-01 | E-GEOD-18881 | biostudies-arrayexpress
Project description:In the phytopathogenic Basidiomcete Ustilago maydis, sexual and pathogenic development are tightly connected and controlled via the b-mating type locus. The b-mating type locus encodes two homeodomain transcription factors, bE and bW, which form an active heterodimeric complex when they are derived from different b-alleles. Rbf1 encodes a zinc-finger transcription factor that is expressed upon formation of an active bE/bW heterodimer. To analyse the dependency of b and rbf1, changes in gene expression were monitored in strain AB31 (Brachmann et al., 2001, Mol Microbiol 42, 1047-1063) and in the derivative AB31Δrbf1 in which rbf1 was deleted. AB31 harbours the active combination bE1 and bW2 under the control of the arabinose-inducible crg1 promoter. Samples were taken 3h, 5h and 12h after induction of bE/bW gene expression. Strain AB32, which harbors the incompatible bE2 and bW2 combination, was used as control.
2010-06-01 | GSE18754 | GEO
Project description:In the phytopathogenic Basidiomcete Ustilago maydis, sexual and pathogenic development are tightly connected and controlled via the b-mating type locus. The b-mating type locus encodes two homeodomain transcription factors, bE and bW, which form an active heterodimeric complex when they are derived from different b-alleles. Rbf1 encodes a zinc-finger transcription factor that is expressed upon formation of an active bE/bW heterodimer. To analyse the dependency of b and rbf1, changes in gene expression were monitored in strain AB31 (Brachmann et al., 2001, Mol Microbiol 42, 1047-1063) and in the derivative AB31Δrbf1 in which rbf1 was deleted. AB31 harbours the active combination bE1 and bW2 under the control of the arabinose-inducible crg1 promoter. Samples were taken 3h, 5h and 12h after induction of bE/bW gene expression. Strain AB32, which harbors the incompatible bE2 and bW2 combination, was used as control. Strains were grown to an OD600 of 0.4-0.6 at 28°C in liquid array medium: 6.25% (w/v) salt solution, 30 mM L-glutamine, 1% (w/v) glucose, pH 7.0 (filter-sterilized). For induction of the bE and bW genes, cells were inoculated in liquid array medium containing 1% (w/v) arabinose instead of glucose as a carbon source. For induction, cells were washed once with inducing medium; time point 0 h of the time course experiments corresponds to the first contact with inducing medium. Experiments were performed in two biological replicates for each time point.
2010-06-01 | E-GEOD-18754 | biostudies-arrayexpress
Project description:Fungal pathogens require the unfolded protein response (UPR) to maintain protein homeostasis of the endoplasmic reticulum (ER) during pathogenic development. In the corn smut fungus Ustilago maydis, pathogenic development is controlled by the a and b mating-type loci. The UPR is specifically activated after plant penetration and required for efficient secretion of effectors and suppression of the plant defense response. The interaction between the UPR regulator Cib1 and the central developmental regulator Clp1 modulates the pathogenic program and triggers fungal colonization of the host plant. By contrast, when activated before plant penetration, the UPR interferes with fungal virulence by reducing expression of bE and bW, the central regulators of pathogenic development encoded by the b mating-type locus. Here, we show that this inhibitory effect results from UPR-mediated suppression of the pheromone response pathway upstream of the b regulatory network. UPR activity prompts dephosphorylation of the pheromone-responsive mitogen-activated protein kinase (MAPK) Kpp2, reducing activity of the pheromone response factor Prf1 that regulates expression of bE and bW Deletion of the dual specificity phosphatase rok1 fully suppressed UPR-dependent inhibition of Kpp2 phosphorylation, formation of infectious filaments, and fungal virulence. Rok1 determines the activity of mating-type signaling pathways and thus the degree of fungal virulence. We propose that UPR-dependent regulation of Rok1 aligns ER physiology with fungal aggressiveness and effector gene expression during biotrophic growth of U. maydis in the host plant.IMPORTANCE The unfolded protein response (UPR) is crucial for endoplasmic reticulum (ER) homeostasis and disease development in fungal pathogens. In the plant-pathogenic fungus Ustilago maydis, the UPR supports fungal proliferation in planta and effector secretion for plant defense suppression. In this study, we uncovered that UPR activity, which is normally restricted to the biotrophic stage in planta, inhibits mating and the formation of infectious filaments by Rok1-dependent dephosphorylation of the pheromone responsive mitogen-activated protein kinase (MAPK) Kpp2. This observation is relevant for understanding how the fungal virulence program is regulated by cellular physiology. UPR-mediated control of mating-type signaling pathways predicts that effector gene expression and the virulence potential are controlled by ER stress levels.
| S-EPMC6918084 | biostudies-literature
Project description:In the phytopathogenic Basidiomcete Ustilago maydis, sexual and pathogenic development are tightly connected and controlled via the b-mating type locus. The b-mating type locus encodes two homeodomain transcription factors, bE and bW, which form an active heterodimeric complex when they are derived from different b-alleles. Rbf1 encodes a zinc-finger transcription factor that is expressed upon formation of an active bE/bW heterodimer. To identify gene regulated by rbf1 independently from b, the b mating type locus was replaced by a copy of rbf1 under control of the arabinose-inducible crg1 promoter (strain CP27). Samples were taken 5h after induction of rbf1 gene expression. Strain JB2, carrying a deletion of the b-locus, was used as control.
2010-06-01 | GSE18756 | GEO
Project description:In the phytopathogenic fungus Ustilago maydis, pheromone-mediated cell fusion is a prerequisite for the generation of the infectious dikaryon. The pheromone signal elevates transcription of the pheromone genes and elicits formation of conjugation hyphae. Cyclic AMP and mitogen-activated protein kinase (MAPK) signaling are involved in this process. The MAPK cascade is presumed to be composed of Ubc4 (MAPK kinase kinase), Fuz7 (MAPK kinase), and Ubc3/Kpp2 (MAPK). We isolated the kpp4 gene and found it to be allelic to ubc4. Epistasis analyses with constitutively active alleles of kpp4 and fuz7 substantiate that Kpp4, Fuz7, and Kpp2/Ubc3 are components of the same module. Moreover, we demonstrate that Fuz7 activates Kpp2 and shows interactions in vitro. Signaling via this cascade regulates expression of pheromone-responsive genes, presumably through acting on the transcription factor Prf1. Interestingly, the same cascade is needed for conjugation tube formation, and this process does not involve Prf1. In addition, fuz7 as well as kpp4 deletion strains are nonpathogenic, while kpp2 deletion mutants are only attenuated in pathogenesis. Here we show that strains expressing the unphosphorylatable allele kpp2(T182A/Y184F) are severely affected in tumor induction and display defects in early infection-related differentiation.
| S-EPMC326639 | biostudies-literature
Project description:Ustilago maydis causes smut disease on corn. Successful infection depends on a number of morphological transitions, such as pheromone-dependent formation of conjugation tubes and the switch to filamentous dikaryotic growth, as well as different types of mycelial structures during growth within the host plant. In order to address the involvement of RNA-binding proteins during this developmental program, we identified 27 open reading frames from the genome sequence encoding potential RNA-binding proteins. They exhibit similarities to RNA-binding proteins with Pumilio homology domains (PUM), the K homology domain (KHD), the double-stranded RNA binding motif (DSRM), and the RNA recognition motif (RRM). For 18 of these genes, we generated replacement mutants in compatible haploid strains. Through analysis of growth behavior, morphology, cyclic AMP response, mating, and pathogenicity, we identified three candidates with aberrant phenotypes. Loss of Khd1, a K homology protein containing three KHDs, resulted in a cold-sensitive growth phenotype. Deletion of khd4 encoding a protein with five KHDs led to abnormal cell morphology, reduced mating, and virulence. rrm4Delta strains were affected in filamentous growth and pathogenicity. Rrm4 is an RRM protein with a so far unique domain organization consisting of three N-terminal RRMs as well as a domain found in the C terminus of poly(A)-binding proteins. These results indicate a role for RNA-binding proteins in regulation of morphology as well as in pathogenic development in U. maydis.
| S-EPMC544158 | biostudies-literature
Project description:Ustilago maydis is a plant-pathogenic fungus that establishes a biotrophic relationship with its host Zea mays. The biotrophic interaction is initiated upon host penetration, and involves expansion of the host plasma membrane around hyphae, which is thought to facilitate the exchange of nutrients and virulence factors. Transcriptional regulators involved in the establishment of an infectious dikaryon and penetration into the host have been identified, however, regulators involved in the post-penetration stages remained to be elucidated. In the study we report the identification of an Ustilago maydis forkhead transcription factor, Fox1, which is exclusively expressed during biotrophic development. Deletion of fox1 results in reduced virulence and impaired tumour development in planta. Microarray analyses of Δfox1-infected plant tissue identified Fox1 as a transcriptional activator, involved in the expression of secreted effectors required for virulence.
2010-12-31 | GSE19591 | GEO
Project description:Ustilago maydis is a plant-pathogenic fungus that establishes a biotrophic relationship with its host Zea mays. The biotrophic interaction is initiated upon host penetration, and involves expansion of the host plasma membrane around hyphae, which is thought to facilitate the exchange of nutrients and virulence factors. Transcriptional regulators involved in the establishment of an infectious dikaryon and penetration into the host have been identified, however, regulators involved in the post-penetration stages remained to be elucidated. In the study we report the identification of an Ustilago maydis forkhead transcription factor, Fox1, which is exclusively expressed during biotrophic development. Deletion of fox1 results in reduced virulence and impaired tumour development in planta. Microarray analyses of Δfox1-infected plant tissue identified Fox1 as a transcriptional activator, involved in the expression of secreted effectors required for virulence. Maize plants were infected with a mixture of either FB1 and FB2 (wild-type), or FB1∆fox1 and FB2∆fox1 crossings, to measure the impact of fox1 on pathogenic development. Early Golden Bantam maize plants were grown in a phytochamber in a 15h/9h light-dark cycle; light period started/ended with 1h ramping of light intensity. Maize plants were kept at 28°C (light) and 20° (dark). Plantlets were individually sown in pots with potting soil (Fruhstorfer Pikiererde) and infected 7 days after sowing, 1 h before end of the light period. Infected leaf tumor material from at least 10 plants was collected 5 days post infection, 1 h before the end of the light period and directly frozen in liquid nitrogen for RNA-extraction. RNA samples were extracted from infected leaf tissue 5 days after infection.
2010-12-31 | E-GEOD-19591 | biostudies-arrayexpress