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Light-dependent functions of the Fusarium fujikuroi CryD DASH cryptochrome in development and secondary metabolism.

ABSTRACT: DASH (Drosophila, Arabidopsis, Synechocystis, human) cryptochromes (cry-DASHs) constitute a subgroup of the photolyase cryptochrome family with diverse light-sensing roles, found in most taxonomical groups. The genome of Fusarium fujikuroi, a phytopathogenic fungus with a rich secondary metabolism, contains a gene encoding a putative cry-DASH, named CryD. The expression of the cryD gene is induced by light in the wild type, but not in mutants of the "white collar" gene wcoA. Targeted ?cryD mutants show light-dependent phenotypic alterations, including changes in morphology and pigmentation, which disappear upon reintroduction of a wild-type cryD allele. In addition to microconidia, the colonies of the ?cryD mutants produced under illumination and nitrogen starvation large septated spores called macroconidia, absent in wild-type colonies. The ?cryD mutants accumulated similar amounts of carotenoids to the control strain under constant illumination, but produced much larger amounts of bikaverin under nitrogen starvation, indicating a repressing role for CryD in this biosynthetic pathway. Additionally, a moderate photoinduction of gibberellin production was exhibited by the wild type but not by the ?cryD mutants. The phenotypic alterations of the ?cryD mutants were only noticeable in the light, as expected from the low expression of cryD in the dark, but did not correlate with mRNA levels for structural genes of the bikaverin or gibberellin biosynthetic pathways, suggesting the participation of CryD in posttranscriptional regulatory mechanisms. This is the first report on the participation of a cry-DASH protein in the regulation of fungal secondary metabolism.

SUBMITTER: Castrillo M

PROVIDER: S-EPMC3623198 | biostudies-literature | 2013 Apr

REPOSITORIES: biostudies-literature

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Light-dependent functions of the Fusarium fujikuroi CryD DASH cryptochrome in development and secondary metabolism.

Castrillo Marta M García-Martínez Jorge J Avalos Javier J

Applied and environmental microbiology 20130215 8

DASH (Drosophila, Arabidopsis, Synechocystis, human) cryptochromes (cry-DASHs) constitute a subgroup of the photolyase cryptochrome family with diverse light-sensing roles, found in most taxonomical groups. The genome of Fusarium fujikuroi, a phytopathogenic fungus with a rich secondary metabolism, contains a gene encoding a putative cry-DASH, named CryD. The expression of the cryD gene is induced by light in the wild type, but not in mutants of the "white collar" gene wcoA. Targeted ΔcryD mutan ...[more]

PMID: 23417004

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Project description:The heterothallic ascomycete Fusarium fujikuroi is a notorious rice pathogen causing super-elongation of plants due to the production of terpene-derived gibberellic acids (GAs) that function as natural plant hormones. Additionally, F. fujikuroi is able to produce a variety of polyketide- and non-ribosomal peptide-derived metabolites such as bikaverins, fusarubins and fusarins as well as metabolites from yet unidentified biosynthetic pathways, e.g. moniliformin. The key enzymes needed for their production belong to the family of polyketide synthases (PKSs) and non-ribosomal peptide synthases (NRPSs) that are generally known to be post-translationally modified by a Sfp-type 4'phosphopantetheinyl transferase (PPTase). In this study we provide evidence that the F. fujikuroi Sfp-type PPTase FfPpt1 is essentially involved in lysine biosynthesis and production of bikaverins, fusarubins and fusarins, but not moniliformin as shown by analytical methods. Concomitantly, targeted Ffppt1 deletion mutants reveal an enhancement of terpene-derived metabolites like GAs and volatile substances such as ?-acorenol. Pathogenicity assays on rice roots using fluorescent labeled wild-type and Ffppt1 mutant strains indicate that lysine biosynthesis and iron acquisition but not PKS and NRPS metabolism is essential for establishment of primary infections of F. fujikuroi. Additionally, FfPpt1 is involved in conidiation and sexual mating recognition possibly by activating PKS- and/or NRPS-derived metabolites that could act as diffusible signals. Furthermore, the effect on iron acquisition of Ffppt1 mutants led us to identify a previously uncharacterized putative third reductive iron uptake system (FfFtr3/FfFet3) that is closely related to the FtrA/FetC system of A. fumigatus. Functional characterization provides evidence that both proteins are involved in iron acquisition and are liable to transcriptional repression of the homolog of the Aspergillus GATA-type transcription factor SreA under iron-replete conditions. Targeted deletion of the first Fusarium homolog of this GATA-type transcription factor-encoding gene, Ffsre1, strongly indicates its involvement in regulation of iron homeostasis and oxidative stress resistance.

Project description:Investigation of whole genome gene expression of the Fusarium fujikuroi wild type IMI58289 under gibberellin-inducing and -repressing conditions. Fusarium fujikuroi is a biotechnologically important fungus due to its almost unique ability to produce gibberellic acids (GAs), a family of phytohormones. The fungus was already described about 100 years ago as the causative agent of Bakanae (foolish seedling) disease of rice. Beside GAs, the fungus is known to produce some pigments and mycotoxins, but for only eight products the biosynthetic genes are known. Here we present a high-quality genome sequence of the first member of the Gibberella fujikuroi species complex (GFC), that allowed de novo genome assembly with 12 scaffolds corresponding to the 12 chromosomes. In this work, we focused on identification of all potential secondary metabolism-related gene clusters and their regulation in response to nitrogen availability by transcriptome, proteome, HPLC-FLPC and ChIP-seq analyses. We show that most of the cluster genes are regulated in a nitrogen-dependent manner, and that expression profiles fit to proteome and ChIP-seq data for some but not all clusters. Comparison with genomes of all available Fusarium species, including the recently sequenced F. mangiferae and F. circinatum, showed only a small number of common gene clusters and provides new insights into the divergence of secondary metabolism in the genus Fusarium. Phylogenetic analyses suggest that some gene clusters were acquired by horizontal gene transfer, while others were present in ancient Fusarim species and have evolved differently by gene duplications and losses. One PKS and one NRPS gene cluster are unique for F. fujikuroi. Their products were identified by combining overexpression of cluster genes with HPLC-FLPC -based product analyses. In planta, expression studies suggest a specific role of the PKS19 product in rice infection. Our results indicate that comparative genomics together with the used genome-wide experimental approaches is a powerful tool to uncover new secondary metabolites and to understand their regulation on the transcript, protein and epigenetic levels. In this study, we hybridized in total 15 microarrays using total RNA recovered from wild-type cultures of F. fujikuroi IMI58289. Two cultures were grown on a 6 mM Gln medium. Additionally, two technical replicates were created. Four cultures were grown on a 60 mM Gln medium. Again, two technical replicates were created. On a 6 mM NO3 medium, three cultures were grown, and two cultures on a 120 mM NO3 medium, with no technical replicates. Each chip measures the expression level of 14,397 genes from F. fujikuroi IMI58289 with eight 60-mer probes.

Project description:Fusarium fujikuroi is a biotechnologically important fungus due to its almost unique ability to produce gibberellic acids (GAs), a family of phytohormones. The fungus was described about 100 years ago as the causative agent of Bakanae (M-bM-^@M-^\foolish seedlingM-bM-^@M-^]) disease of rice. Apart from GAs, the fungus is known to produce pigments and mycotoxins, but the biosynthetic genes are known for only eight products. Here we present a high-quality genome sequence of the first member of the Gibberella fujikuroi species complex (GFC) that allowed de novo genome assembly with 12 scaffolds corresponding to the 12 chromosomes. In this work we focused on identification of all potential secondary metabolism-related gene clusters and their regulation in response to nitrogen availability by transcriptome, proteome, HPLC-FTMS and ChIP-seq analyses. We show that most of the cluster genes are regulated in a nitrogen-dependent manner, and that expression profiles fit to proteome and ChIP-seq data for some but not all clusters. Comparison with genomes of all available Fusarium species, including the recently sequenced F. mangiferae and F. circinatum, showed only a small number of common gene clusters and provides new insights into the divergence of secondary metabolism in the genus Fusarium. Phylogenetic analyses suggest that some gene clusters were acquired by horizontal gene transfer, while others were present in ancient Fusarim species and have evolved differently by gene duplications and losses. One polyketide synthase (PKS) and one non-ribosomal peptide synthetase (NRPS) gene cluster are unique for F. fujikuroi. Their products were identified by combining overexpression of cluster genes with HPLC-FTMS-based analyses. In planta expression studies suggest a specific role of the PKS19 product in rice infection. Our results indicate that comparative genomics together with the used genome-wide experimental approaches is a powerful tool to uncover new secondary metabolites and to understand their regulation at the transcriptional, translational and epigenetic levels. Examination of 3 different histone modifications, with 2 growth conditions for one of the modifications (Total of 4 samples)

Dataset Information

Light-dependent functions of the Fusarium fujikuroi CryD DASH cryptochrome in development and secondary metabolism.

Publications

Light-dependent functions of the Fusarium fujikuroi CryD DASH cryptochrome in development and secondary metabolism.

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