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.
