title: Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites.
abstract: The fungus Fusarium fujikuroi causes "bakanae" disease of rice due to its ability to produce gibberellins (GAs), but it is also known for producing harmful mycotoxins. However, the genetic capacity for the whole arsenal of natural compounds and their role in the fungus' interaction with rice remained unknown. Here, we present a high-quality genome sequence of F. fujikuroi that was assembled into 12 scaffolds corresponding to the 12 chromosomes described for the fungus. We used the genome sequence along with ChIP-seq, transcriptome, proteome, and HPLC-FTMS-based metabolome analyses to identify the potential secondary metabolite biosynthetic gene clusters and to examine their regulation in response to nitrogen availability and plant signals. The results indicate that expression of most but not all gene clusters correlate with proteome and ChIP-seq data. Comparison of the F. fujikuroi genome to those of six other fusaria revealed that only a small number of gene clusters are conserved among these species, thus providing new insights into the divergence of secondary metabolism in the genus Fusarium. Noteworthy, GA biosynthetic genes are present in some related species, but GA biosynthesis is limited to F. fujikuroi, suggesting that this provides a selective advantage during infection of the preferred host plant rice. Among the genome sequences analyzed, one cluster that includes a polyketide synthase gene (PKS19) and another that includes a non-ribosomal peptide synthetase gene (NRPS31) are unique to F. fujikuroi. The metabolites derived from these clusters were identified by HPLC-FTMS-based analyses of engineered F. fujikuroi strains overexpressing cluster genes. In planta expression studies suggest a specific role for the PKS19-derived product during rice infection. Thus, our results indicate that combined comparative genomics and genome-wide experimental analyses identified novel genes and secondary metabolites that contribute to the evolutionary success of F. fujikuroi as a rice pathogen.
authors.affiliation: Institut für Biologie und Biotechnologie der Pflanzen, Molecular Biology and Biotechnology of Fungi, Westfälische Wilhelms-Universität Münster, Münster, Germany.
authors.forename: Philipp
authors.initials: P
authors.lastname: Wiemann
authors.forename: Christian M K
authors.initials: CM
authors.lastname: Sieber
authors.forename: Katharina W
authors.initials: KW
authors.lastname: von Bargen
authors.forename: Lena
authors.initials: L
authors.lastname: Studt
authors.forename: Eva-Maria
authors.initials: EM
authors.lastname: Niehaus
authors.forename: Jose J
authors.initials: JJ
authors.lastname: Espino
authors.forename: Kathleen
authors.initials: K
authors.lastname: Huß
authors.forename: Caroline B
authors.initials: CB
authors.lastname: Michielse
authors.forename: Sabine
authors.initials: S
authors.lastname: Albermann
authors.forename: Dominik
authors.initials: D
authors.lastname: Wagner
authors.forename: Sonja V
authors.initials: SV
authors.lastname: Bergner
authors.forename: Lanelle R
authors.initials: LR
authors.lastname: Connolly
authors.forename: Andreas
authors.initials: A
authors.lastname: Fischer
authors.forename: Gunter
authors.initials: G
authors.lastname: Reuter
authors.forename: Karin
authors.initials: K
authors.lastname: Kleigrewe
authors.forename: Till
authors.initials: T
authors.lastname: Bald
authors.forename: Brenda D
authors.initials: BD
authors.lastname: Wingfield
authors.forename: Ron
authors.initials: R
authors.lastname: Ophir
authors.forename: Stanley
authors.initials: S
authors.lastname: Freeman
authors.forename: Michael
authors.initials: M
authors.lastname: Hippler
authors.forename: Kristina M
authors.initials: KM
authors.lastname: Smith
authors.forename: Daren W
authors.initials: DW
authors.lastname: Brown
authors.forename: Robert H
authors.initials: RH
authors.lastname: Proctor
authors.forename: Martin
authors.initials: M
authors.lastname: Münsterkötter
authors.forename: Michael
authors.initials: M
authors.lastname: Freitag
authors.forename: Hans-Ulrich
authors.initials: HU
authors.lastname: Humpf
authors.forename: Ulrich
authors.initials: U
authors.lastname: Güldener
authors.forename: Bettina
authors.initials: B
authors.lastname: Tudzynski
mesh_terms: D005656:Fungal Proteins / Q000235:genetics* / Q000378:metabolism*; D005670:Fusarium / Q000235:genetics* / Q000378:metabolism*; D016681:Genome, Fungal / Q000502:physiology*; D055106:Genome-Wide Association Study; D012275:Oryza / Q000382:microbiology; D010935:Plant Diseases / Q000382:microbiology
chemical_list: D005656:Fungal Proteins