Research Article: Deciphering the Cryptic Genome: Genome-wide Analyses of the Rice Pathogen Fusarium fujikuroi Reveal Complex Regulation of Secondary Metabolism and Novel Metabolites

Date Published: June 27, 2013

Publisher: Public Library of Science

Author(s): Philipp Wiemann, Christian M. K. Sieber, Katharina W. von Bargen, Lena Studt, Eva-Maria Niehaus, Jose J. Espino, Kathleen Huß, Caroline B. Michielse, Sabine Albermann, Dominik Wagner, Sonja V. Bergner, Lanelle R. Connolly, Andreas Fischer, Gunter Reuter, Karin Kleigrewe, Till Bald, Brenda D. Wingfield, Ron Ophir, Stanley Freeman, Michael Hippler, Kristina M. Smith, Daren W. Brown, Robert H. Proctor, Martin Münsterkötter, Michael Freitag, Hans-Ulrich Humpf, Ulrich Güldener, Bettina Tudzynski, Aaron P. Mitchell.

http://doi.org/10.1371/journal.ppat.1003475

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.

Partial Text

The genus Fusarium is one of the most important groups of phytopathogenic fungi. They infect a broad spectrum of crops worldwide and are responsible for huge economic losses due to yield reductions and mycotoxin contamination. The Gibberella fujikuroi species complex (GFC) constitutes a monophyletic but diverse subgroup of over 50 Fusarium species with similar morphological features. The complex is divided into the African, American and Asian clades, according to DNA-based phylogenetic analyses [1]–[3] (Figure 1A).

 

Source:

http://doi.org/10.1371/journal.ppat.1003475

 

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