Dataset Information

Comparative transcriptome and proteome analysis reveals a global impact of the nitrogen regulators AreA and AreB on secondary metabolism in Fusarium fujikuroi.

ABSTRACT: The biosynthesis of multiple secondary metabolites in the phytopathogenic ascomycete Fusarium fujikuroi is strongly affected by nitrogen availability. Here, we present the first genome-wide transcriptome and proteome analysis that compared the wild type and deletion mutants of the two major nitrogen regulators AreA and AreB. We show that AreB acts not simply as an antagonist of AreA counteracting the expression of AreA target genes as suggested based on the yeast model. Both GATA transcription factors affect a large and diverse set of common as well as specific target genes and proteins, acting as activators and repressors. We demonstrate that AreA and AreB are not only involved in fungal nitrogen metabolism, but also in the control of several complex cellular processes like carbon metabolism, transport and secondary metabolism. We show that both GATA transcription factors can be considered as master regulators of secondary metabolism as they affect the expression of more than half of the 47 putative secondary metabolite clusters identified in the genome of F. fujikuroi. While AreA acts as a positive regulator of many clusters under nitrogen-limiting conditions, AreB is able to activate and repress gene clusters (e.g. bikaverin) under nitrogen limitation and sufficiency. In addition, ChIP analyses revealed that loss of AreA or AreB causes histone modifications at some of the regulated gene clusters.

SUBMITTER: Pfannmuller A

PROVIDER: S-EPMC5404775 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Comparative transcriptome and proteome analysis reveals a global impact of the nitrogen regulators AreA and AreB on secondary metabolism in Fusarium fujikuroi.

Pfannmüller Andreas A Leufken Johannes J Studt Lena L Michielse Caroline B CB Sieber Christian M K CMK Güldener Ulrich U Hawat Susan S Hippler Michael M Fufezan Christian C Tudzynski Bettina B

PloS one 20170425 4

The biosynthesis of multiple secondary metabolites in the phytopathogenic ascomycete Fusarium fujikuroi is strongly affected by nitrogen availability. Here, we present the first genome-wide transcriptome and proteome analysis that compared the wild type and deletion mutants of the two major nitrogen regulators AreA and AreB. We show that AreB acts not simply as an antagonist of AreA counteracting the expression of AreA target genes as suggested based on the yeast model. Both GATA transcription f ...[more]

PMID: 28441411

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Project description:BackgroundBakanae is a seedborne disease caused by Fusarium fujikuroi. Rice seedlings emerging from infected seeds can show diverse symptoms such as elongated and slender stem and leaves, pale coloring, a large leaf angle, stunted growth and even death. Little is known about rice defense mechanisms at early stages of disease development.ResultsThis study focused on investigating early defenses against F. fujikuroi in a susceptible cultivar, Zerawchanica karatals (ZK), and a resistant cultivar, Tainung 67 (TNG67). Quantitative PCR revealed that F. fujikuroi colonizes the root and stem but not leaf tissues. Illumina sequencing was conducted to analyze the stem transcriptomes of F. fujikuroi-inoculated and mock-inoculated ZK and TNG67 plants collected at 7 days post inoculation (dpi). More differentially expressed genes (DEGs) were identified in ZK (n = 169) than TNG67 (n = 118), and gene ontology terms related to transcription factor activity and phosphorylation were specifically enriched in ZK DEGs. Among the complex phytohormone biosynthesis and signaling pathways, only DEGs involved in the jasmonic acid (JA) signaling pathway were identified. Fourteen DEGs encoding pattern-recognition receptors, transcription factors, and JA signaling pathway components were validated by performing quantitative reverse transcription PCR analysis of individual plants. Significant repression of jasmonate ZIM-domain (JAZ) genes (OsJAZ9, OsJAZ10, and OsJAZ13) at 3 dpi and 7 dpi in both cultivars, indicated the activation of JA signaling during early interactions between rice and F. fujikuroi. Differential expression was not detected for salicylic acid marker genes encoding phenylalanine ammonia-lyase 1 and non-expressor of pathogenesis-related genes 1. Moreover, while MeJA did not affect the viability of F. fujikuroi, MeJA treatment of rice seeds (prior to or after inoculation) alleviated and delayed bakanae disease development in susceptible ZK.ConclusionsDifferent from previous transcriptome studies, which analyzed the leaves of infected plants, this study provides insights into defense-related gene expression patterns in F. fujikuroi-colonized rice stem tissues. Twelve out of the 14 selected DEGs were for the first time shown to be associated with disease resistance, and JA-mediated resistance was identified as a crucial component of rice defense against F. fujikuroi. Detailed mechanisms underlying the JA-mediated bakanae resistance and the novel defense-related DEGs are worthy of further investigation.

Project description:BACKGROUND:Bakanae disease, caused by the fungus Fusarium fujikuroi, occurs widely throughout Asia and Europe and sporadically in other rice production areas. Recent changes in climate and cropping patterns have aggravated this disease. To gain a better understanding of the molecular mechanisms of rice bakanae disease resistance, we employed a 6-plex tandem mass tag approach for relative quantitative proteomic comparison of infected and uninfected rice seedlings 7?days post-inoculation with two genotypes: the resistant genotype 93-11 and the susceptible genotype Nipponbare. RESULTS:In total, 123 (77.2% up-regulated, 22.8% down-regulated) and 91 (94.5% up-regulated, 5.5% down-regulated) differentially expressed proteins (DEPs) accumulated in 93-11 and Nipponbare, respectively. Only 11 DEPs were both shared by the two genotypes. Clustering results showed that the protein regulation trends for the two genotypes were highly contrasting, which suggested obviously different interaction mechanisms of the host and the pathogen between 93 and 11 and Nipponbare. Further analysis showed that a noticeable aquaporin, PIP2-2, was sharply upregulated with a fold change (FC) of 109.2 in 93-11, which might be related to pathogen defense and the execution of bakanae disease resistance. Certain antifungal proteins were regulated in both 93-11 and Nipponbare with moderate FCs. These proteins might participate in protecting the cellular integrity required for basic growth of the susceptible genotype. Correlation analysis between the transcriptome and proteome revealed that Pearson correlation coefficients of R?=?0.677 (P?=?0.0005) and R?=?-?0.097 (P?=?0.702) were obtained for 93-11 and Nipponbare, respectively. Our findings raised an intriguing result that a significant positive correlation only in the resistant genotype, while no correlation was found in the susceptible genotype. The differences in codon usage was hypothesized for the cause of the result. CONCLUSIONS:Quantitative proteomic analysis of the rice genotypes 93-11and Nipponbare after F. fujikuroi infection revealed that the aquaporin protein PIP2-2 might execute bakanae disease resistance. The difference in the correlation between the transcriptome and proteome might be due to the differences in codon usage between 93-11and Nipponbare. Overall, the protein regulation trends observed under bakanae disease stress are highly contrasting, and the molecular mechanisms of disease defense are obviously different between 93 and 11 and Nipponbare. In summary, these findings deepen our understanding of the functions of proteins induced by bakanae disease and the mechanisms of rice bakanae disease resistance.

Project description:Histone modifications have been shown to be crucial for secondary metabolism in various filamentous fungi. Here we studied the influence of histone acetylation on secondary metabolite production in the phytopathogenic fungus Fusarium fujikuroi, a known producer of several secondary metabolites including pigments and mycotoxins. Deletion of the classical HDACs FfHdF1, FfHdF2 and FfHdF3 indicated that FfHdF1 and FfHdF2 are major regulators of secondary metabolism, whereas FfHdF3 is involved in developmental processes but dispensable for secondary metabolite production in F. fujikuroi. Microarray analysis with the major HDAC FfHdF2 revealed differential regulation of several secondary metabolite gene clusters, subsequently verified by a combination of chemical and biological approaches. These results indicate that HDACs are responsible for gene silencing but also gene activation. Chromatin immunoprecipitation assays with M-NM-^TffhdF2 revealed significant alterations regarding the acetylation state in the landscape of secondary metabolite gene clusters thereby providing insights into the regulatory mechanism. In addition, the class I HDAC FfHdF1 also has major impact on secondary metabolism in F. fujikuroi. Furthermore, deletion of both ffhdF1 and ffhdF2 resulted in de-repression of secondary metabolites under normally repressing conditions. Thus, manipulation of HDAC encoding genes might provide a powerful tool for the activation of cryptic secondary metabolites. Investigation of whole genome gene expression of the Fusarium fujikuroi wild type IMI58289, M-NM-^TffhdF2 mutant under nitrogen starvation and nitrogen sufficient conditions. In this study we hybridized in total 12 microarrays using total RNA recovered from a wild-type culture of F. fujikuroi IMI58289 and M-NM-^TffhdF2 mutant culture. All cultures were grown on a 6 mM Gln (10%) and a 60 mM Gln medium (100%). For each combination of culture and medium a biological replicate was created. Each chip measures the expression level of 14,397 genes from F. fujikuroi IMI58289 with eight 60-mer probes.

Dataset Information

Comparative transcriptome and proteome analysis reveals a global impact of the nitrogen regulators AreA and AreB on secondary metabolism in Fusarium fujikuroi.

Publications

Comparative transcriptome and proteome analysis reveals a global impact of the nitrogen regulators AreA and AreB on secondary metabolism in Fusarium fujikuroi.

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