Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites.
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 wi...
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oai:doaj.org-article:64ccef6ac774468e98cdc339e19a91412021-11-18T06:05:27ZDeciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites.1553-73661553-737410.1371/journal.ppat.1003475https://doaj.org/article/64ccef6ac774468e98cdc339e19a91412013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23825955/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374The 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.Philipp WiemannChristian M K SieberKatharina W von BargenLena StudtEva-Maria NiehausJose J EspinoKathleen HußCaroline B MichielseSabine AlbermannDominik WagnerSonja V BergnerLanelle R ConnollyAndreas FischerGunter ReuterKarin KleigreweTill BaldBrenda D WingfieldRon OphirStanley FreemanMichael HipplerKristina M SmithDaren W BrownRobert H ProctorMartin MünsterkötterMichael FreitagHans-Ulrich HumpfUlrich GüldenerBettina TudzynskiPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 9, Iss 6, p e1003475 (2013) |
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Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 |
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Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 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 Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. |
| description |
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. |
| format |
article |
| author |
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 |
| author_facet |
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 |
| author_sort |
Philipp Wiemann |
| title |
Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. |
| title_short |
Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. |
| title_full |
Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. |
| title_fullStr |
Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. |
| title_full_unstemmed |
Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. |
| title_sort |
deciphering the cryptic genome: genome-wide analyses of the rice pathogen fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2013 |
| url |
https://doaj.org/article/64ccef6ac774468e98cdc339e19a9141 |
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