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The regulatory and transcriptional landscape associated with carbon utilization in a filamentous fungus.

ABSTRACT: Filamentous fungi, such as Neurospora crassa, are very efficient in deconstructing plant biomass by the secretion of an arsenal of plant cell wall-degrading enzymes, by remodeling metabolism to accommodate production of secreted enzymes, and by enabling transport and intracellular utilization of plant biomass components. Although a number of enzymes and transcriptional regulators involved in plant biomass utilization have been identified, how filamentous fungi sense and integrate nutritional information encoded in the plant cell wall into a regulatory hierarchy for optimal utilization of complex carbon sources is not understood. Here, we performed transcriptional profiling of N. crassa on 40 different carbon sources, including plant biomass, to provide data on how fungi sense simple to complex carbohydrates. From these data, we identified regulatory factors in N. crassa and characterized one (PDR-2) associated with pectin utilization and one with pectin/hemicellulose utilization (ARA-1). Using in vitro DNA affinity purification sequencing (DAP-seq), we identified direct targets of transcription factors involved in regulating genes encoding plant cell wall-degrading enzymes. In particular, our data clarified the role of the transcription factor VIB-1 in the regulation of genes encoding plant cell wall-degrading enzymes and nutrient scavenging and revealed a major role of the carbon catabolite repressor CRE-1 in regulating the expression of major facilitator transporter genes. These data contribute to a more complete understanding of cross talk between transcription factors and their target genes, which are involved in regulating nutrient sensing and plant biomass utilization on a global level.

SUBMITTER: Wu VW

PROVIDER: S-EPMC7084071 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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The regulatory and transcriptional landscape associated with carbon utilization in a filamentous fungus.

Wu Vincent W VW Thieme Nils N Huberman Lori B LB Dietschmann Axel A Kowbel David J DJ Lee Juna J Calhoun Sara S Singan Vasanth R VR Lipzen Anna A Xiong Yi Y Monti Remo R Blow Matthew J MJ O'Malley Ronan C RC Grigoriev Igor V IV Benz J Philipp JP Glass N Louise NL

Proceedings of the National Academy of Sciences of the United States of America 20200228 11

Filamentous fungi, such as <i>Neurospora crassa</i>, are very efficient in deconstructing plant biomass by the secretion of an arsenal of plant cell wall-degrading enzymes, by remodeling metabolism to accommodate production of secreted enzymes, and by enabling transport and intracellular utilization of plant biomass components. Although a number of enzymes and transcriptional regulators involved in plant biomass utilization have been identified, how filamentous fungi sense and integrate nutritio ...[more]

PMID: 32111691

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Project description:BackgroundResearch on filamentous fungi emphasized the remarkable redundancy in genes encoding hydrolytic enzymes, the similarities but also the large differences in their expression, especially through the role of the XlnR/XYR1 transcriptional activator. The purpose of this study was to evaluate the specificities of the industrial fungus Talaromyces versatilis, getting clues into the role of XlnR and the importance of glucose repression at the transcriptional level, to provide further levers for cocktail production.ResultsBy studying a set of 62 redundant genes representative of several categories of enzymes, our results underlined the huge plasticity of transcriptional responses when changing nutritional status. As a general trend, the more heterogeneous the substrate, the more efficient to trigger activation. Genetic modifications of xlnR led to significant reorganisation of transcriptional patterns. Just a minimal set of genes actually fitted in a simplistic model of regulation by a transcriptional activator, and this under specific substrates. On the contrary, the diversity of xlnR+ versus ΔxlnR responses illustrated the existence of complex and unpredicted patterns of co-regulated genes that were highly dependent on the culture condition, even between genes that encode members of a functional category of enzymes. They notably revealed a dual, substrate-dependant repressor-activator role of XlnR, with counter-intuitive transcripts regulations that targeted specific genes. About glucose, it appeared as a formal repressive sugar as we observed a massive repression of most genes upon glucose addition to the mycelium grown on wheat straw. However, we also noticed a positive role of this sugar on the basal expression of a few genes, (notably those encoding cellulases), showing again the strong dependence of these regulatory mechanisms upon promoter and nutritional contexts.ConclusionsThe diversity of transcriptional patterns appeared to be the rule, while common and stable behaviour, both within gene families and with fungal literature, the exception. The setup of a new biotechnological process to reach optimized, if not customized expression patterns of enzymes, hence appeared tricky just relying on published data that can lead, in the best scenario, to approximate trends. We instead encourage preliminary experimental assays, carried out in the context of interest to reassess gene responses, as a mandatory step before thinking in (genetic) strategies for the improvement of enzyme production in fungi.

Project description:Fungi use oxylipins (oxidized lipids) as signaling molecules to induce asexual development. These molecules play an essential role in the response to wounding, exerting a protective effect against plant pathogens, and are part of the inflammatory process in animals. However, the physiological and molecular mechanisms triggered by oxylipins that lead to asexual development in fungi are not well understood. Using a genetic approach, mass spectrometry, and phenotypic analysis, we describe the functional role of a patatin-like phospholipase (plp1) and a unique lipoxygenase (lox1) in the response to injury in the model fungus Trichoderma atroviride. lox1 and plp1 are co-expressed and regulated by damage signaling and sensing components. Phenotypic analysis revealed an essential defect in the emergence of aerial hyphae in the lox1 and plp1 null mutant strains, blocking injury-induced conidiation. In addition, functional loss analysis demonstrated that both genes are essential for wound-associated linoleic acid-derived oxylipin 13-hydroxy-9Z,11E-octadecadienoic acid (13-HODE) production and the transcriptional reprogramming required for conidiation. T. atroviride requires LOX1 and PLP1 to induce transcription factors involved in asexual development such as brlA, hox2, and azf1 homologs at the early stages of the response and at a later stage to activate lipid metabolism and the structural proteins involved in aerial mycelium emergence. Our study shows how the cooperative function of lox1 and plp1, during the response to wounding, regulates the molecular and physiological processes of damaged-sensitized cells that lead to reproductive aerial mycelium development and consequently, ensure survival through asexual reproduction.IMPORTANCEIn addition to being considered a biocontrol agent, the fungus Trichoderma atroviride is a relevant model for studying mechanisms of response to injury conserved in plants and animals that opens a new landscape in relation to regeneration and cell differentiation mechanisms. Here, we reveal the co-functionality of a lipoxygenase and a patatin-like phospholipase co-expressed in response to wounding in fungi. This pair of enzymes produces oxidized lipids that can function as signaling molecules or oxidative stress signals that, in ascomycetes, induce asexual development. Furthermore, we determined that both genes participate in the regulation of the synthesis of 13-HODE and the establishment of the physiological responses necessary for the formation of reproductive aerial mycelium ultimately leading to asexual development. Our results suggest an injury-induced pathway to produce oxylipins and uncovered physiological mechanisms regulated by LOX1 and PLP1 to induce conidiation, opening new hypotheses for the novo regeneration mechanisms of filamentous fungi.

Dataset Information

The regulatory and transcriptional landscape associated with carbon utilization in a filamentous fungus.

Publications

The regulatory and transcriptional landscape associated with carbon utilization in a filamentous fungus.

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