Aspects of the Neurospora crassa Sulfur Starvation Response Are Revealed by Transcriptional Profiling and DNA Affinity Purification Sequencing

Huberman, Lori B.; Wu, V.; Lee, Juna; Daum, Chris; O’Malley, Ronan; Glass, N. Louise

doi:10.1128/msphere.00564-21

Cited by 5 publications

(7 citation statements)

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“…Previous studies on N. crassa , Penicillium expansum , and A. nidulans have shown that the deletion of cys-3 / metR significantly reduces the transcript levels of sulfur assimilation genes and their enzyme activities, aligning with the observations in this study ( 21 , 37 , 38 ). In addition, in N. crassa , random sequence oligonucleotides and DAP-seq analysis revealed CYS3 binding motifs as 5′-ATBRCGCCATC-3′ and 5′- ATGGCGCCAT -3′ ( 25 , 41 ), which exhibit high similarity to the motif analysis results in this study. Overall, these findings demonstrate that Fgbzip007 is a functional ortholog of the CYS3/METR and, like typical bZIP proteins, plays a significant role in a wide range of mechanisms including nutrient utilization and stress response.…”

Section: Discussionsupporting

confidence: 80%

“…Our results showing that Fgbzip007 interacts with FGSG_08463 and FGSG_08528 involved in sulfur metabolism led us to identify the genes encoding enzymes involved in the sulfur assimilation pathway in F. graminearum . Based on previous reports that identified genes for the sulfur assimilation pathway in N. crassa and A. nidulans ( 25 , 26 ), we identified seven genes, including FGSG_08463 and FGSG_08528, in this study that encode sulfate permease, sulfate adenylyltransferase, adenylyl-sulfate kinase, phosphoadenosine phosphosulfate (PAPS) reductase, and sulfite reductase using BLASTp analysis: CYS13, CYS14, CYS11, ADSK1, CYS5, CYS2 , and CYS4 ( Table 1 ). When we analyzed the transcript levels of these genes under sulfur-deprived conditions, all genes were upregulated in the wild-type strain 2 h after being transferred to a sulfur-deficient condition ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“…( A ) Schematic of sulfur assimilation pathway in F. graminearum and expression profiles of sulfur assimilation pathway genes under sulfur-deprived conditions. The schematic of the sulfur assimilation pathway in F. graminearum is modified from the pathway in the previous study of N. crassa ( 25 ). APS, adenosine 5′-phosphosulfate; PAPS, 3′-phosphoadenosine-5′-phosphosulfate.…”

Section: Resultsmentioning

confidence: 99%

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Sulfur metabolism-mediated fungal glutathione biosynthesis is essential for oxidative stress resistance and pathogenicity in the plant pathogenic fungus Fusarium graminearum

Park,

Han,

Lee

et al. 2024

mBio

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The oxidative stress response is required for plant pathogens to endure host-derived oxidative stress during infection. Previously, we identified the eight transcription factors (TFs) involved in the oxidative stress response in the plant pathogenic fungus Fusarium graminearum and found that of these TFs, the deletion of FgbZIP007 caused hypersensitivity to oxidative stress. However, the underlying mechanisms of Fgbzip007 are not fully understood. Based on chromatin immunoprecipitation followed by sequencing (ChIP-seq) analysis, we found the regulons of Fgbzip007, and further genetic studies demonstrated that Fgbzip007 is a key regulator for sulfur assimilation. The deletion strains of FgbZIP007 and its regulons exhibited low level of glutathione biosynthesis, which led to characterize glutathione biosynthesis. Fgbzip007-mediated sulfur assimilation is required for glutathione biosynthesis, which is essential for oxidative stress resistance and pathogenicity in F. graminearum . Although the reduced resistance of glutathione-deficient mutants against oxidative stress was restored by overexpression of FCA7 , encoding a core peroxidase, but not on pathogenicity, suggesting that glutathione in pathogenesis is independent of antioxidant properties. This study characterized the function of genes of glutathione biosynthesis, provides specific insight into how Fgbzip007 regulates pathogenesis in F. graminearum , and establishes a genetic framework for the molecular dissection of a TF Fgbzip007 with the integration of pathogen responses to oxidative stress. IMPORTANCE Fusarium graminearum is a destructive fungal pathogen that causes Fusarium head blight (FHB) on a wide range of cereal crops. To control fungal diseases, it is essential to comprehend the pathogenic mechanisms that enable fungi to overcome host defenses during infection. Pathogens require an oxidative stress response to overcome host-derived oxidative stress. Here, we identify the underlying mechanisms of the Fgbzip007-mediated oxidative stress response in F. graminearum . ChIP-seq and subsequent genetic analyses revealed that the role of glutathione in pathogenesis is not dependent on antioxidant functions in F. graminearum . Altogether, this study establishes a comprehensive framework for the Fgbzip007 regulon on pathogenicity and oxidative stress responses, offering a new perspective on the role of glutathione in pathogenicity.

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Section: Discussionsupporting

confidence: 80%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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Sulfur metabolism-mediated fungal glutathione biosynthesis is essential for oxidative stress resistance and pathogenicity in the plant pathogenic fungus Fusarium graminearum

Park,

Han,

Lee

et al. 2024

mBio

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“… 86 , 88 Two genes viz., cys-13 (permease I) and cys14 (permease II) which encode the N. crassa sulfate transporters are of high affinity in nature. 87 , 89 Sulfur sources, like sulfate or methionine, regulate both the genes at the transcriptional level. Under sulfur starvation, both genes have been shown to be highly expressed.…”

Section: Sulfate Permeases In Fungimentioning

confidence: 99%

Sulfur nutrition and its role in plant growth and development

Narayan

Kumar

Yadav

et al. 2022

Plant Signaling & Behavior

113

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Sulfur is one of the essential nutrients that is required for the adequate growth and development of plants. Sulfur is a structural component of protein disulfide bonds, amino acids, vitamins, and cofactors. Most of the sulfur in soil is present in organic matter and hence not accessible to the plants. Anionic form of sulfur (SO 4 2− ) is the primary source of sulfur for plants that are generally present in minimal amounts in the soil. It is water-soluble, so readily leaches out of the soil. Sulfur and sulfur-containing compounds act as signaling molecules in stress management as well as normal metabolic processes. They also take part in crosstalk of complex signaling network as a mediator molecule. Plants uptake sulfate directly from the soil by using their dedicated sulfate transporters. In addition, plants also use the sulfur transporter of a symbiotically associated organism like bacteria and fungi to uptake sulfur from the soil especially under sulfur depleted conditions. So, sulfur is a very important component of plant metabolism and its analysis with different dimensions is highly required to improve the overall well-being of plants, and dependent animals as well as human beings. The deficiency of sulfur leads to stunted growth of plants and ultimately loss of yield. In this review, we have focused on sulfur nutrition, uptake, transport, and inter-organismic transfer to host plants. Given the strong potential for agricultural use of sulfur sources and their applications, we cover what is known about sulfur impact on the plant health. We identify opportunities to expand our understanding of how the application of soil microbes like AMF or other root endophytic fungi affects plant sulfur uptake and in turn plant growth and development.

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“…retain the ability to bind DNA and act as the main (and possibly the sole) regulators controlling the pathway 33,34 . In all these species Met4 is absolutely required for methionine biosynthesis, and its disruption results in methionine auxotrophy 25,[32][33][34] . Nothing is known about sulphur assimilation and cysteine/methionine biosynthesis in C. parapsilosis.…”

Section: Introductionmentioning

confidence: 99%

Alternative sulphur metabolism in the fungal pathogen Candida parapsilosis

Lombardi,

Salzberg,

Cinnéide

et al. 2024

Preprint

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Candida parapsilosis is an opportunistic fungal pathogen commonly isolated from the environment and associated with nosocomial infection outbreaks worldwide. We describe here the construction of a large collection of gene disruptions, which we use to dissect the network regulating the assimilation of sulphur in C. parapsilosis. We identify a wide array of transporters/enzymes involved in the assimilation of organosulfur compounds. We find that, unlike in other yeasts, the two paralogous transcription factors Met4 and Met28 play divergent roles in sulphur acquisition. Surprisingly, Met28 – and not Met4 – controls the assimilation of inorganic sulphur (sulphate) and the synthesis of cysteine/methionine, whereas Met4 and the transcription factor Met32 induce the expression of genes required for assimilation of inorganic sulphate. Divergent regulation of sulphur metabolism is likely to be important for scavenging essential sulphur in the diverse environments that C. parapsilosis can colonize.

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Aspects of the Neurospora crassa Sulfur Starvation Response Are Revealed by Transcriptional Profiling and DNA Affinity Purification Sequencing

Abstract: Identification of nutrients present in the environment is a challenge common to all organisms. Sulfur is an important nutrient source found in proteins, lipids, and electron carriers that are required for the survival of filamentous fungi such as Neurospora crassa .

Cited by 5 publications

References 50 publications

Sulfur metabolism-mediated fungal glutathione biosynthesis is essential for oxidative stress resistance and pathogenicity in the plant pathogenic fungus Fusarium graminearum

Sulfur metabolism-mediated fungal glutathione biosynthesis is essential for oxidative stress resistance and pathogenicity in the plant pathogenic fungus Fusarium graminearum

Sulfur nutrition and its role in plant growth and development

Alternative sulphur metabolism in the fungal pathogen Candida parapsilosis

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