Dataset Information

Regulation of gene expression by ambient pH in filamentous fungi and yeasts.

ABSTRACT: Life, as we know it, is water based. Exposure to hydroxonium and hydroxide ions is constant and ubiquitous, and the evolutionary pressure to respond appropriately to these ions is likely to be intense. Fungi respond to their environments by tailoring their output of activities destined for the cell surface or beyond to the ambient pH. We are beginning to glimpse how they sense ambient pH and transmit this information to the transcription factor, whose roles ensure that a suitable collection of gene products will be made. Although relatively little is known about pH signal transduction itself, its consequences for the cognate transcription factor are much clearer. Intriguingly, homologues of components of this system mediating the regulation of fungal gene expression by ambient pH are to be found in the animal kingdom. The potential applied importance of this regulatory system lies in its key role in fungal pathogenicity of animals and plants and in its control of fungal production of toxins, antibiotics, and secreted enzymes.

SUBMITTER: Penalva MA

PROVIDER: S-EPMC120796 | biostudies-literature | 2002 Sep

REPOSITORIES: biostudies-literature

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Regulation of gene expression by ambient pH in filamentous fungi and yeasts.

Peñalva Miguel A MA Arst Herbert N HN

Microbiology and molecular biology reviews : MMBR 20020901 3

Life, as we know it, is water based. Exposure to hydroxonium and hydroxide ions is constant and ubiquitous, and the evolutionary pressure to respond appropriately to these ions is likely to be intense. Fungi respond to their environments by tailoring their output of activities destined for the cell surface or beyond to the ambient pH. We are beginning to glimpse how they sense ambient pH and transmit this information to the transcription factor, whose roles ensure that a suitable collection of g ...[more]

PMID: 12208998

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Project description:Fungi are known to utilize transcriptional regulation of genes that encode efflux transporters to detoxify xenobiotics; however, to date it is unknown how fungi transcriptionally regulate and coordinate different phases of detoxification system (phase I, modification; phase II, conjugation; and phase III, secretion). Here we present evidence of an evolutionary convergence between the fungal and mammalian lineages, whereby xenobiotic detoxification genes (phase I coding for cytochrome P450 monooxygenases [CYP450s] and phase III coding for ATP-binding cassette [ABC] efflux transporters) are transcriptionally regulated by structurally unrelated proteins. Following next-generation RNA sequencing (RNA-seq) analyses of a filamentous fungus, Sclerotinia homoeocarpa, the causal agent of dollar spot on turfgrasses, a multidrug resistant (MDR) field strain was found to overexpress phase I and III genes, coding for CYP450s and ABC transporters for xenobiotic detoxification. Furthermore, there was confirmation of a gain-of-function mutation of the fungus-specific transcription factor S. homoeocarpa XDR1 (ShXDR1), which is responsible for constitutive and induced overexpression of the phase I and III genes, resulting in resistance to multiple classes of fungicidal chemicals. This fungal pathogen detoxifies xenobiotics through coordinated transcriptional control of CYP450s, biotransforming xenobiotics with different substrate specificities and ABC transporters, excreting a broad spectrum of xenobiotics or biotransformed metabolites. A Botrytis cinerea strain harboring the mutated ShXDR1 showed increased expression of phase I (BcCYP65) and III (BcatrD) genes, resulting in resistance to fungicides. This indicates the regulatory system is conserved in filamentous fungi. This molecular genetic mechanism for xenobiotic detoxification in fungi holds potential for facilitating discovery of new antifungal drugs and further studies of convergent and divergent evolution of xenobiotic detoxification in eukaryote lineages.IMPORTANCE Emerging multidrug resistance (MDR) in pathogenic filamentous fungi is a significant threat to human health and agricultural production. Understanding mechanisms of MDR is essential to combating fungal pathogens; however, there is still limited information on MDR mechanisms conferred by xenobiotic detoxification. Here, we report for the first time that overexpression of phase I drug-metabolizing monooxygenases (cytochrome P450s) and phase III ATP-binding cassette efflux transporters is regulated by a gain-of-function mutation in the fungus-specific transcription factor in the MDR strains of the filamentous plant-pathogenic fungus Sclerotinia homoeocarpa This study establishes a novel molecular mechanism of MDR through the xenobiotic detoxification pathway in filamentous fungi, which may facilitate the discovery of new antifungal drugs to control pathogenic fungi.

Project description:BackgroundAutomated gene-calling is still an error-prone process, particularly for the highly plastic genomes of fungal species. Improvement through quality control and manual curation of gene models is a time-consuming process that requires skilled biologists and is only marginally performed. The wealth of available fungal genomes has not yet been exploited by an automated method that applies quality control of gene models in order to obtain more accurate genome annotations.ResultsWe provide a novel method named alignment-based fungal gene prediction (ABFGP) that is particularly suitable for plastic genomes like those of fungi. It can assess gene models on a gene-by-gene basis making use of informant gene loci. Its performance was benchmarked on 6,965 gene models confirmed by full-length unigenes from ten different fungi. 79.4% of all gene models were correctly predicted by ABFGP. It improves the output of ab initio gene prediction software due to a higher sensitivity and precision for all gene model components. Applicability of the method was shown by revisiting the annotations of six different fungi, using gene loci from up to 29 fungal genomes as informants. Between 7,231 and 8,337 genes were assessed by ABFGP and for each genome between 1,724 and 3,505 gene model revisions were proposed. The reliability of the proposed gene models is assessed by an a posteriori introspection procedure of each intron and exon in the multiple gene model alignment. The total number and type of proposed gene model revisions in the six fungal genomes is correlated to the quality of the genome assembly, and to sequencing strategies used in the sequencing centre, highlighting different types of errors in different annotation pipelines. The ABFGP method is particularly successful in discovering sequence errors and/or disruptive mutations causing truncated and erroneous gene models.ConclusionsThe ABFGP method is an accurate and fully automated quality control method for fungal gene catalogues that can be easily implemented into existing annotation pipelines. With the exponential release of new genomes, the ABFGP method will help decreasing the number of gene models that require additional manual curation.

Dataset Information

Regulation of gene expression by ambient pH in filamentous fungi and yeasts.

Publications

Regulation of gene expression by ambient pH in filamentous fungi and yeasts.

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