Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites.
| Title: | Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. |
|---|---|
| Authors: | Wiemann P; Institut für Biologie und Biotechnologie der Pflanzen, Molecular Biology and Biotechnology of Fungi, Westfälische Wilhelms-Universität Münster, Münster, Germany.; Sieber CM; von Bargen KW; Studt L; Niehaus EM; Espino JJ; Huß K; Michielse CB; Albermann S; Wagner D; Bergner SV; Connolly LR; Fischer A; Reuter G; Kleigrewe K; Bald T; Wingfield BD; Ophir R; Freeman S; Hippler M; Smith KM; Brown DW; Proctor RH; Münsterkötter M; Freitag M; Humpf HU; Güldener U; Tudzynski B |
| Source: | PLoS pathogens [PLoS Pathog] 2013; Vol. 9 (6), pp. e1003475. Date of Electronic Publication: 2013 Jun 27. |
| Publication Type: | Journal Article; Research Support, Non-U.S. Gov't |
| Language: | English |
| Journal Info: | Publisher: Public Library of Science Country of Publication: United States NLM ID: 101238921 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1553-7374 (Electronic) Linking ISSN: 15537366 NLM ISO Abbreviation: PLoS Pathog Subsets: MEDLINE |
| Imprint Name(s): | Original Publication: San Francisco, CA : Public Library of Science, c2005- |
| MeSH Terms: | Fungal Proteins/*genetics ; Fungal Proteins/*metabolism ; Fusarium/*genetics ; Fusarium/*metabolism ; Genome, Fungal/*physiology; Oryza/microbiology ; Plant Diseases/microbiology ; Genome-Wide Association Study |
| 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. |
| References: | Mycol Res. 2004 Jul;108(Pt 7):815-22. (PMID: 15446715); Fungal Genet Biol. 1998 Dec;25(3):157-70. (PMID: 9917370); Methods Enzymol. 2012;517:325-41. (PMID: 23084946); Int J Evol Biol. 2011;2011:423821. (PMID: 21716743); Methods Mol Biol. 2009;537:39-64. (PMID: 19378139); Methods Enzymol. 2012;515:359-77. (PMID: 22999182); Bioinformatics. 2009 Jul 15;25(14):1754-60. (PMID: 19451168); Genome Res. 2008 Aug;18(8):1362-8. (PMID: 18502942); Proteomics. 2011 May;11(9):1814-23. (PMID: 21432999); Nat Biotechnol. 2008 Oct;26(10):1161-8. (PMID: 18820685); Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W435-9. (PMID: 16845043); Fungal Genet Biol. 2008 Jun;45(6):1016-26. (PMID: 18375156); Mol Gen Genet. 1999 Feb;261(1):106-14. (PMID: 10071216); Nucleic Acids Res. 2011 Jan;39(Database issue):D637-9. (PMID: 21051345); Genome Biol. 2011;12(4):R40. (PMID: 21501500); Fungal Genet Biol. 2011 Jan;48(1):62-9. (PMID: 20659575); J Agric Food Chem. 2006 Sep 20;54(19):7083-8. (PMID: 16968066); Nature. 2005 Dec 22;438(7071):1105-15. (PMID: 16372000); Proc Natl Acad Sci U S A. 2011 Aug 23;108(34):14282-7. (PMID: 21825172); Mol Microbiol. 2007 Nov;66(3):713-26. (PMID: 17919289); J Agric Food Chem. 2012 Aug 29;60(34):8350-5. (PMID: 22877497); Phytopathology. 2009 Jun;99(6):775-81. (PMID: 19453238); Biochim Biophys Acta. 1980 May 7;629(2):382-90. (PMID: 7388041); Nat Biotechnol. 2012 Oct;30(10):918-20. (PMID: 23051804); G3 (Bethesda). 2013 Feb;3(2):369-78. (PMID: 23390613); J Mol Biol. 2000 Jul 21;300(4):1005-16. (PMID: 10891285); Mol Microbiol. 2010 Jun;76(6):1376-86. (PMID: 20132440); Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15670-5. (PMID: 14676319); Mycotoxin Res. 2012 Feb;28(1):37-43. (PMID: 23605981); Appl Environ Microbiol. 2008 Dec;74(24):7790-801. (PMID: 18952870); Nucleic Acids Res. 2004 Oct 14;32(18):5539-45. (PMID: 15486203); Curr Genet. 2011 Jun;57(3):177-89. (PMID: 21246198); Cell. 2009 Aug 21;138(4):795-806. (PMID: 19664813); Chembiochem. 2013 Feb 11;14(3):311-5. (PMID: 23335243); Appl Environ Microbiol. 2012 Oct;78(20):7258-66. (PMID: 22865073); Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2008 Sep;25(9):1158-65. (PMID: 19238625); Genetics. 1996 May;143(1):175-89. (PMID: 8722773); Mol Plant Pathol. 2001 Jul 1;2(4):229-39. (PMID: 20573011); Biostatistics. 2003 Apr;4(2):249-64. (PMID: 12925520); Cytogenet Genome Res. 2005;110(1-4):462-7. (PMID: 16093699); Phytochemistry. 2009 Oct-Nov;70(15-16):1876-93. (PMID: 19560174); Nucleic Acids Res. 1997 Mar 1;25(5):955-64. (PMID: 9023104); Fungal Genet Biol. 2004 Oct;41(10):897-910. (PMID: 15341912); Bioorg Med Chem Lett. 2012 Jul 1;22(13):4338-40. (PMID: 22633689); Phytochemistry. 2005 Jun;66(11):1296-311. (PMID: 15925394); Genome Biol Evol. 2012;4(3):289-93. (PMID: 22294497); Bioinformatics. 2005 Jun;21 Suppl 1:i351-8. (PMID: 15961478); Appl Environ Microbiol. 2008 Sep;74(17):5325-39. (PMID: 18567680); Genetics. 2007 Oct;177(2):1217-20. (PMID: 17660534); Nat Methods. 2011 Sep 29;8(10):785-6. (PMID: 21959131); Appl Microbiol. 1959 Sep;7:301-3. (PMID: 13814121); Mol Microbiol. 2009 May;72(4):931-46. (PMID: 19400779); Curr Biol. 2011 Jan 25;21(2):134-9. (PMID: 21194949); Syst Biol. 2008 Aug;57(4):613-27. (PMID: 18709599); BMC Genomics. 2012 Oct 02;13:519. (PMID: 23031507); Phytopathology. 1999 Jun;89(6):456-61. (PMID: 18944716); Annu Rev Genomics Hum Genet. 2006;7:301-13. (PMID: 16756479); BMC Evol Biol. 2008 Dec 03;8:328. (PMID: 19055762); Mol Plant Microbe Interact. 2007 Aug;20(8):922-33. (PMID: 17722696); Genetics. 2010 Dec;186(4):1207-16. (PMID: 20876559); J Am Chem Soc. 2009 Mar 4;131(8):2965-70. (PMID: 19199437); Curr Opin Plant Biol. 2006 Aug;9(4):371-5. (PMID: 16713733); Cell Res. 2011 Mar;21(3):381-95. (PMID: 21321607); Nat Chem Biol. 2009 Jul;5(7):462-4. (PMID: 19448638); Nucleic Acids Res. 1999 Jan 15;27(2):573-80. (PMID: 9862982); Mol Microbiol. 2012 Oct;86(2):314-30. (PMID: 22882998); Fungal Genet Biol. 2002 Nov;37(2):134-48. (PMID: 12409099); Nat Biotechnol. 2007 Feb;25(2):221-31. (PMID: 17259976); PLoS One. 2013;8(1):e53729. (PMID: 23308280); Mol Cell Biol. 1991 Nov;11(11):5746-55. (PMID: 1922075); Gene. 1992 Jan 2;110(1):119-22. (PMID: 1544568); Appl Environ Microbiol. 2009 Jan;75(2):405-13. (PMID: 19047398); Bioinformatics. 2011 Apr 15;27(8):1183-4. (PMID: 21325302); Bioinformatics. 2010 Oct 1;26(19):2363-7. (PMID: 20688976); Bioinformatics. 2009 Apr 1;25(7):964-6. (PMID: 19193729); Fungal Genet Biol. 2008 Jun;45(6):947-53. (PMID: 18440841); Genome Res. 2000 Apr;10(4):516-22. (PMID: 10779491); Curr Protoc Bioinformatics. 2009 Dec;Chapter 9:Unit 9.9. (PMID: 19957275); Mol Biol Evol. 2011 Oct;28(10):2731-9. (PMID: 21546353); Bioinformatics. 2012 Apr 1;28(7):1052-3. (PMID: 22302572); J Antibiot (Tokyo). 1992 Aug;45(8):1273-7. (PMID: 1399848); Nucleic Acids Res. 2010 Jan;38(Database issue):D223-6. (PMID: 19906725); Mol Microbiol. 2010 Apr;76(2):456-66. (PMID: 20233305); Proc Natl Acad Sci U S A. 2006 Jul 5;103(27):10352-10357. (PMID: 16801547); Biosci Biotechnol Biochem. 2006 Mar;70(3):583-90. (PMID: 16556972); mBio. 2012 Sep 04;3(5):e00259-12. (PMID: 22951933); Mol Cell Biol. 2011 Jun;31(12):2528-42. (PMID: 21505064); Fungal Genet Biol. 2012 Jul;49(7):567-77. (PMID: 22626844); Fungal Genet Biol. 2009 May;46(5):353-64. (PMID: 19285149); PLoS Genet. 2013;9(2):e1003323. (PMID: 23468653); Nucleic Acids Res. 2009 Jan;37(Database issue):D408-11. (PMID: 18940859); J Mol Biol. 1994 Oct 14;243(1):116-22. (PMID: 7932733); Nucleic Acids Res. 2002 Jun 1;30(11):2478-83. (PMID: 12034836); Methods Mol Biol. 2012;944:1-22. (PMID: 23065605); PLoS One. 2012;7(5):e37519. (PMID: 22662164); Nucleic Acids Res. 2009 Jan;37(1):289-97. (PMID: 19042974); Cancer Res. 2000 Nov 1;60(21):6068-74. (PMID: 11085529); PLoS Genet. 2011 Aug;7(8):e1002230. (PMID: 21876677); Nucleic Acids Res. 2001 May 1;29(9):e45. (PMID: 11328886); Int J Food Microbiol. 2012 Apr 16;155(3):128-36. (PMID: 22377171); Fungal Genet Biol. 2008 Oct;45(10):1393-403. (PMID: 18694840); Genome Res. 2008 Dec;18(12):1979-90. (PMID: 18757608); Appl Environ Microbiol. 2012 Jun;78(12):4468-80. (PMID: 22492438); J Agric Food Chem. 2012 May 30;60(21):5497-505. (PMID: 22540270); BMC Bioinformatics. 2007 Nov 30;8:466. (PMID: 18047679); J Agric Food Chem. 2006 Mar 22;54(6):2424-30. (PMID: 16536629); Phytochemistry. 2010 Aug;71(11-12):1322-31. (PMID: 20570295); Curr Genet. 2003 Apr;43(1):54-61. (PMID: 12684845); BMC Bioinformatics. 2008 Oct 27;9:456. (PMID: 18954438); J Mol Biol. 2001 Jan 19;305(3):567-80. (PMID: 11152613); Genome Res. 2004 Jul;14(7):1394-403. (PMID: 15231754); Plant J. 2001 Feb;25(3):305-14. (PMID: 11208022); Nucleic Acids Res. 2011 Mar;39(5):e27. (PMID: 21131282); Fungal Genet Biol. 2012 Jun;49(6):483-97. (PMID: 22503771); Mol Plant Microbe Interact. 2008 Jan;21(1):87-97. (PMID: 18052886); Org Biomol Chem. 2008 Jun 7;6(11):1895-7. (PMID: 18480899); Bioinformatics. 2004 Jun 12;20(9):1466-7. (PMID: 14976030); J Biol Chem. 2004 Jun 11;279(24):25075-84. (PMID: 15037621); PLoS Genet. 2013;9(1):e1003233. (PMID: 23357949); Mycologia. 2005 Jan-Feb;97(1):191-201. (PMID: 16389971); Mol Microbiol. 2010 Nov;78(3):720-38. (PMID: 20969648); Mol Microbiol. 2013 Jan;87(1):49-65. (PMID: 23106229); PLoS Genet. 2010 Apr 08;6(4):e1000891. (PMID: 20386741); Eukaryot Cell. 2005 Nov;4(11):1926-33. (PMID: 16278459); PLoS Genet. 2009 Aug;5(8):e1000618. (PMID: 19714214); Nucleic Acids Res. 2007 Jul;35(Web Server issue):W265-8. (PMID: 17485477); Curr Genet. 2007 Jan;51(1):43-58. (PMID: 17043871); Genome Res. 2002 Oct;12(10):1599-610. (PMID: 12368253); Food Addit Contam. 2007 Oct;24(10):1076-87. (PMID: 17886180); Fungal Biol. 2012 Feb;116(2):318-31. (PMID: 22289777); PLoS Genet. 2011 Jan 06;7(1):e1001264. (PMID: 21253567); J Proteome Res. 2004 Sep-Oct;3(5):958-64. (PMID: 15473683); Appl Environ Microbiol. 1999 Jun;65(6):2558-64. (PMID: 10347043); Nucleic Acids Res. 1992 May 11;20(9):2380. (PMID: 1594460); Mol Cell Proteomics. 2011 Jan;10(1):R110.000133. (PMID: 20716697); Nature. 2010 Mar 18;464(7287):367-73. (PMID: 20237561); Nat Rev Microbiol. 2013 Jan;11(1):21-32. (PMID: 23178386); Nat Prod Rep. 2010 Jan;27(1):11-22. (PMID: 20024091); Proteomics. 2012 Jan;12(1):21-31. (PMID: 22065615); Methods Mol Biol. 2011;722:179-89. (PMID: 21590421); Syst Biol. 2010 May;59(3):307-21. (PMID: 20525638); Mol Microbiol. 2003 Feb;47(4):975-91. (PMID: 12581353); Eukaryot Cell. 2007 Jul;6(7):1210-8. (PMID: 17483290); Chromosome Res. 2012 Jul;20(5):635-56. (PMID: 22752455); Nat Genet. 2012 Sep;44(9):1060-5. (PMID: 22885923); J Agric Food Chem. 2011 Oct 12;59(19):10470-6. (PMID: 21894895); Mol Cell Proteomics. 2010 Jul;9(7):1514-32. (PMID: 20190198); Fungal Genet Biol. 2012 Jul;49(7):521-32. (PMID: 22652150) |
| Grant Information: | R01 GM097637 United States GM NIGMS NIH HHS |
| Substance Nomenclature: | 0 (Fungal Proteins) |
| Entry Date(s): | Date Created: 20130705 Date Completed: 20140117 Latest Revision: 20240324 |
| Update Code: | 20260130 |
| PubMed Central ID: | PMC3694855 |
| DOI: | 10.1371/journal.ppat.1003475 |
| PMID: | 23825955 |
| Database: | MEDLINE |
Journal Article; Research Support, Non-U.S. Gov't