The WOPR protein Ros1 is a master regulator of sporogenesis and effector gene expression in the maize pathogen Ustilago maydis
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ABSTRACT:
ORGANISM(S): Mycosarcoma maydis
PROVIDER: GSE76231 | GEO | 2016/06/24
SECONDARY ACCESSION(S): PRJNA306676
REPOSITORIES: GEO
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Project description:The biotrophic basidiomycete fungus Ustilago maydis causes smut disease in maize. Hallmarks of the disease are large tumors that develop on all aerial parts of the host in which dark pigmented teliospores are formed. We have identified a member of the WOPR family of transcription factors, Ros1, as major regulator of spore formation in U. maydis. ros1 expression is induced only late during infection and hence Ros1 is neither involved in plant colonization of dikaryotic fungal hyphae nor in plant tumor formation. However, during late stages of infection Ros1 is essential for fungal karyogamy, massive proliferation of diploid fungal cells and spore formation. Premature expression of ros1 revealed that Ros1 counteracts the b-dependent filamentation program and induces morphological alterations resembling the early steps of sporogenesis. Transcriptional profiling and ChIP-seq analyses uncovered that Ros1 remodels expression of about 30% of all U. maydis genes with 40% of these being direct targets. In total the expression of 80 transcription factor genes is controlled by Ros1. Four of the upregulated transcription factor genes were deleted and two of the mutants were affected in spore development. A large number of b-dependent genes were differentially regulated by Ros1, suggesting substantial changes in this regulatory cascade that controls filamentation and pathogenic development. Interestingly, 128 genes encoding secreted effectors involved in the establishment of biotrophic development were downregulated by Ros1 while a set of 70 "late effectors" was upregulated. These results indicate that Ros1 is a master regulator of late development in U. maydis and show that the biotrophic interaction during sporogenesis involves a drastic shift in expression of the fungal effectome including the downregulation of effectors that are essential during early stages of infection.
| S-EPMC4917244 | biostudies-literature
Project description:This SuperSeries is composed of the SubSeries listed below. Refer to individual Series
2016-06-24 | E-GEOD-76231 | biostudies-arrayexpress
Project description:Goals: characterization of the transcription factor Ros1 in Ustilago maydis Methods: generation of deletion mutants, microscopic observations, ectopic expression of ros1, identification of Ros1 regulated genes by RNAseq and ChIP sequencing Results: Ros1 is not involved in plant colonization but is essential to trigger sporogenesis during late stages of infection. Premature expression of ros1 revealed that Ros1 counteracts the b-dependent filamentation program and induces morphological alterations resembling the early steps of sporogenesis. Transcriptional profiling and ChIP seq analyses revealed that Ros1 affects the expression of about 30 % of all U. maydis genes with 40% being direct targets. Cell wall remodeling and plasma membrane modifications are among the processes affected by Ros1 dependent regulation. Interestingly a large number of b-dependent genes including transcription factors and effector genes involved in biotrophy establishment were downregulated by Ros1 while a subset of novel “late effectors” were upregulated. Taken together our results indicate that Ros1 is a master regulator of sporogenesis in U. maydis and that the switch to sporogenesis is accompanied by the differential regulation of 75% of the effector genes.
2016-06-24 | GSE76230 | GEO
Project description:Goals: characterization of the transcription factor Ros1 in Ustilago maydis Methods: generation of deletion mutants, microscopic observations, ectopic expression of ros1, identification of Ros1 regulated genes by RNAseq and ChIP sequencing Results: Ros1 is not involved in plant colonization but is essential to trigger sporogenesis during late stages of infection. Premature expression of ros1 revealed that Ros1 counteracts the b-dependent filamentation program and induces morphological alterations resembling the early steps of sporogenesis. Transcriptional profiling and ChIP seq analyses revealed that Ros1 affects the expression of about 30 % of all U. maydis genes with 40% being direct targets. Cell wall remodeling and plasma membrane modifications are among the processes affected by Ros1 dependent regulation. Interestingly a large number of b-dependent genes including transcription factors and effector genes involved in biotrophy establishment were downregulated by Ros1 while a subset of novel “late effectors” were upregulated. Taken together our results indicate that Ros1 is a master regulator of sporogenesis in U. maydis and that the switch to sporogenesis is accompanied by the differential regulation of 75% of the effector genes.
2016-06-24 | GSE76229 | GEO
Project description:Goals: characterization of the transcription factor Ros1 in Ustilago maydis Methods: generation of deletion mutants, microscopic observations, ectopic expression of ros1, identification of Ros1 regulated genes by RNAseq and ChIP sequencing Results: Ros1 is not involved in plant colonization but is essential to trigger sporogenesis during late stages of infection. Premature expression of ros1 revealed that Ros1 counteracts the b-dependent filamentation program and induces morphological alterations resembling the early steps of sporogenesis. Transcriptional profiling and ChIP seq analyses revealed that Ros1 affects the expression of about 30 % of all U. maydis genes with 40% being direct targets. Cell wall remodeling and plasma membrane modifications are among the processes affected by Ros1 dependent regulation. Interestingly a large number of b-dependent genes including transcription factors and effector genes involved in biotrophy establishment were downregulated by Ros1 while a subset of novel â??late effectorsâ?? were upregulated. Taken together our results indicate that Ros1 is a master regulator of sporogenesis in U. maydis and that the switch to sporogenesis is accompanied by the differential regulation of 75% of the effector genes. Two samples corresponding to plant material infected with either U. maydis wild type strains FB1 x FB2 or the ros1 deletion strains FB1Dros1 x FB2Dros1 were analyzed in triplicate.
2016-06-24 | E-GEOD-76229 | biostudies-arrayexpress
Project description:Goals: characterization of the transcription factor Ros1 in Ustilago maydis Methods: generation of deletion mutants, microscopic observations, ectopic expression of ros1, identification of Ros1 regulated genes by RNAseq and ChIP sequencing Results: Ros1 is not involved in plant colonization but is essential to trigger sporogenesis during late stages of infection. Premature expression of ros1 revealed that Ros1 counteracts the b-dependent filamentation program and induces morphological alterations resembling the early steps of sporogenesis. Transcriptional profiling and ChIP seq analyses revealed that Ros1 affects the expression of about 30 % of all U. maydis genes with 40% being direct targets. Cell wall remodeling and plasma membrane modifications are among the processes affected by Ros1 dependent regulation. Interestingly a large number of b-dependent genes including transcription factors and effector genes involved in biotrophy establishment were downregulated by Ros1 while a subset of novel â??late effectorsâ?? were upregulated. Taken together our results indicate that Ros1 is a master regulator of sporogenesis in U. maydis and that the switch to sporogenesis is accompanied by the differential regulation of 75% of the effector genes. 4 samples were analyzed in triplicate. The first two samples correspond to input and output DNA obtained from ChIP carried out on plant material infected with U. maydis strains expressing Ros1 with an HA tag. The other two other samples correspond to input and output DNA from ChIP carried out on plant material infected with U. maydis strains expressing Ros1 without a tag (control samples).
2016-06-24 | E-GEOD-76230 | biostudies-arrayexpress
Project description:The WOPR protein Ros1 is a master regulator of sporogenesis and effector gene expression in the maize pathogen Ustilago maydis
| PRJNA306676 | ENA
Project description:The biotrophic fungus Ustilago maydis causes smut disease in maize with characteristic tumor formation and anthocyanin induction. Here, we show that anthocyanin biosynthesis is induced by the virulence promoting secreted effector protein Tin2. Tin2 protein functions inside plant cells where it interacts with maize protein kinase ZmTTK1. Tin2 masks a ubiquitin-proteasome degradation motif in ZmTTK1, thus stabilizing the active kinase. Active ZmTTK1 controls activation of genes in the anthocyanin biosynthesis pathway. Without Tin2, enhanced lignin biosynthesis is observed in infected tissue and vascular bundles show strong lignification. This is presumably limiting access of fungal hyphae to nutrients needed for massive proliferation. Consistent with this assertion, we observe that maize brown midrib mutants affected in lignin biosynthesis are hypersensitive to U. maydis infection. We speculate that Tin2 rewires metabolites into the anthocyanin pathway to lower their availability for other defense responses. DOI: http://dx.doi.org/10.7554/eLife.01355.001.
| S-EPMC3904489 | biostudies-literature
Project description:The biotrophic pathogen Ustilago maydis, the causative agent of corn smut disease, infects one of the most important crops worldwide - Zea mays. To successfully colonize its host, U. maydis secretes proteins, known as effectors, that suppress plant defense responses and facilitate the establishment of biotrophy. In this work, we describe the U. maydis effector protein Cce1. Cce1 is essential for virulence and is upregulated during infection. Through microscopic analysis and in vitro assays, we show that Cce1 is secreted from hyphae during filamentous growth of the fungus. Strikingly, Δcce1 mutants are blocked at early stages of infection and induce callose deposition as a plant defense response. Cce1 is highly conserved among smut fungi and the Ustilago bromivora ortholog complemented the virulence defect of the SG200Δcce1 deletion strain. These data indicate that Cce1 is a core effector with apoplastic localization that is essential for U. maydis to infect its host.
| S-EPMC6638113 | biostudies-literature
Project description:To cause disease in maize, the biotrophic fungus Ustilago maydis secretes a large arsenal of effector proteins. Here, we functionally characterize the repetitive effector Rsp3 (repetitive secreted protein 3), which shows length polymorphisms in field isolates and is highly expressed during biotrophic stages. Rsp3 is required for virulence and anthocyanin accumulation. During biotrophic growth, Rsp3 decorates the hyphal surface and interacts with at least two secreted maize DUF26-domain family proteins (designated AFP1 and AFP2). AFP1 binds mannose and displays antifungal activity against the rsp3 mutant but not against a strain constitutively expressing rsp3. Maize plants silenced for AFP1 and AFP2 partially rescue the virulence defect of rsp3 mutants, suggesting that blocking the antifungal activity of AFP1 and AFP2 by the Rsp3 effector is an important virulence function. Rsp3 orthologs are present in all sequenced smut fungi, and the ortholog from Sporisorium reilianum can complement the rsp3 mutant of U. maydis, suggesting a novel widespread fungal protection mechanism.
| S-EPMC5923269 | biostudies-literature