Deciphering the cryptic genome : genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites

摘要

The fungus Fusarium fujikuroi causes ‘‘bakanae’’ disease of rice due to its ability to produce gibberellins (GAs), but it is alsoknown for producing harmful mycotoxins. However, the genetic capacity for the whole arsenal of natural compounds andtheir 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 thegenome sequence along with ChIP-seq, transcriptome, proteome, and HPLC-FTMS-based metabolome analyses to identifythe potential secondary metabolite biosynthetic gene clusters and to examine their regulation in response to nitrogenavailability and plant signals. The results indicate that expression of most but not all gene clusters correlate with proteomeand ChIP-seq data. Comparison of the F. fujikuroi genome to those of six other fusaria revealed that only a small number ofgene clusters are conserved among these species, thus providing new insights into the divergence of secondarymetabolism in the genus Fusarium. Noteworthy, GA biosynthetic genes are present in some related species, but GAbiosynthesis is limited to F. fujikuroi, suggesting that this provides a selective advantage during infection of the preferredhost plant rice. Among the genome sequences analyzed, one cluster that includes a polyketide synthase gene (PKS19) andanother that includes a non-ribosomal peptide synthetase gene (NRPS31) are unique to F. fujikuroi. The metabolites derivedfrom these clusters were identified by HPLC-FTMS-based analyses of engineered F. fujikuroi strains overexpressing clustergenes. In planta expression studies suggest a specific role for the PKS19-derived product during rice infection. Thus, ourresults indicate that combined comparative genomics and genome-wide experimental analyses identified novel genes andsecondary metabolites that contribute to the evolutionary success of F. fujikuroi as a rice pathogen.