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

PLoS Pathogens

Hans-Ulrich Humpf¹  Andreas Fischer¹  Daren W. Brown¹  Ron Ophir²  Michael Hippler³  Sabine Albermann⁴  Caroline B. Michielse⁴  Kathleen Huß⁴  Jose J. Espino⁴  Sonja V. Bergner⁴  Philipp Wiemann⁴  Dominik Wagner⁴  Lena Studt⁴  Brenda D. Wingfield⁵  Lanelle R. Connolly⁵  Kristina M. Smith⁵  Gunter Reuter⁶  Karin Kleigrewe⁶  Ulrich Güldener⁷  Till Bald⁷  Eva-Maria Niehaus⁷  Katharina W. von Bargen⁷  Michael Freitag⁸  Christian M. K. Sieber⁸  Bettina Tudzynski⁸  Stanley Freeman⁹  Robert H. Proctor^1,10  Martin Münsterkötter^1,10 

[1] Department of Biochemistry and Biophysics, Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon, United States of America;Department of Genetics, University of Pretoria, Hatfield, Pretoria, South Africa;Department of Plant Pathology, Agricultural Research Organization (ARO), The Volcani Center, Bet-Dagan, Israel;Institut für Biologie und Biotechnologie der Pflanzen, Molecular Biology and Biotechnology of Fungi, Westfälische Wilhelms-Universität Münster, Münster, Germany;Institut für Biologie und Biotechnologie der Pflanzen, Plant Biochemistry and Biotechnology, Westfälische Wilhelms-Universität Münster, Münster, Germany;Institut of Genetics/Developmental Genetics, Martin-Luther-Universität Halle-Wittenberg, Halle, Germany;Institute for Food Chemistry, Westfälische Wilhelms-Universität Münster, Corrensstraße 45, Münster, Germany;Institute of Bioinformatics and Systems Biology, Helmholtz Zentrum München, German Research Center for Environmental Health (GmbH), Neuherberg, Germany;Institute of Plant Sciences, Genomics, Agricultural Research Organization (ARO), The Volcani Center, Bet-Dagan, Israel;National Center for Agricultural Utilization Research, United States Department of Agriculture, Peoria, Illinois, United States of America

关键词: Fusarium;    Gibberellins;    Fungal genomics;    Gene expression;    Rice;    Comparative genomics;    Fungi;    Fungal genetics;   

DOI  :  10.1371/journal.ppat.1003475

学科分类：生物科学（综合）

来源: Public Library of Science

【 摘 要 】

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.

【 授权许可】

CC BY