Unravelling the biosynthesis of pyriculol in the rice blast fungus Magnaporthe oryzae.

Stefan Jacob, Thomas Grötsch, Andrew J Foster, Anja Schüffler, Patrick H Rieger, Louis P Sandjo, Johannes C Liermann, Till Opatz, Eckhard Thines
Author Information
  1. Stefan Jacob: Institut für Biotechnologie und Wirkstoff-Forschung gGmbH (IBWF), Erwin-Schrödinger Str. 56, D-67663 Kaiserslautern, Germany.
  2. Thomas Grötsch: Institut für Biotechnologie und Wirkstoff-Forschung gGmbH (IBWF), Erwin-Schrödinger Str. 56, D-67663 Kaiserslautern, Germany.
  3. Andrew J Foster: Institut für Biotechnologie und Wirkstoff-Forschung gGmbH (IBWF), Erwin-Schrödinger Str. 56, D-67663 Kaiserslautern, Germany.
  4. Anja Schüffler: Institut für Biotechnologie und Wirkstoff-Forschung gGmbH (IBWF), Erwin-Schrödinger Str. 56, D-67663 Kaiserslautern, Germany.
  5. Patrick H Rieger: Institut für Biotechnologie und Wirkstoff-Forschung gGmbH (IBWF), Erwin-Schrödinger Str. 56, D-67663 Kaiserslautern, Germany.
  6. Louis P Sandjo: Institute of Organic Chemistry, Johannes Gutenberg University of Mainz, Duesbergweg 10-14, D-55128 Mainz, Germany.
  7. Johannes C Liermann: Institute of Organic Chemistry, Johannes Gutenberg University of Mainz, Duesbergweg 10-14, D-55128 Mainz, Germany.
  8. Till Opatz: Institute of Organic Chemistry, Johannes Gutenberg University of Mainz, Duesbergweg 10-14, D-55128 Mainz, Germany.
  9. Eckhard Thines: Institut für Mikrobiologie und Weinforschung, Johannes Gutenberg University of Mainz, Johann-Joachim-Becherweg 15, D-55128 Mainz, Germany.

Abstract

Pyriculol was isolated from the rice blast fungus Magnaporthe oryzae and found to induce lesion formation on rice leaves. These findings suggest that it could be involved in virulence. The gene MoPKS19 was identified to encode a polyketide synthase essential for the production of the polyketide pyriculol in the rice blast fungus M. oryzae. The transcript abundance of MoPKS19 correlates with the biosynthesis rate of pyriculol in a time-dependent manner. Furthermore, gene inactivation of MoPKS19 resulted in a mutant unable to produce pyriculol, pyriculariol and their dihydro derivatives. Inactivation of a putative oxidase-encoding gene MoC19OXR1, which was found to be located in the genome close to MoPKS19, resulted in a mutant exclusively producing dihydropyriculol and dihydropyriculariol. By contrast, overexpression of MoC19OXR1 resulted in a mutant strain only producing pyriculol. The MoPKS19 cluster, furthermore, comprises two transcription factors MoC19TRF1 and MoC19TRF2, which were both found individually to act as negative regulators repressing gene expression of MoPKS19. Additionally, extracts of ΔMopks19 and ΔMoC19oxr1 made from axenic cultures failed to induce lesions on rice leaves compared to extracts of the wild-type strain. Consequently, pyriculol and its isomer pyriculariol appear to be the only lesion-inducing secondary metabolites produced by M. oryzae wild-type (MoWT) under these culture conditions. Interestingly, the mutants unable to produce pyriculol and pyriculariol were as pathogenic as MoWT, demonstrating that pyriculol is not required for infection.

References

  1. Chem Sci. 2015 Aug 1;6(8):4837-4845 [PMID: 29142718]
  2. Genomics. 2013 Jun;101(6):354-61 [PMID: 23583668]
  3. Mol Biol Evol. 1987 Jul;4(4):406-25 [PMID: 3447015]
  4. Curr Opin Microbiol. 2016 Dec;34:147-153 [PMID: 27816794]
  5. Nat Commun. 2015 Oct 27;6:8758 [PMID: 26503170]
  6. Microbiologyopen. 2014 Oct;3(5):668-87 [PMID: 25103193]
  7. Plant J. 2009 Sep;59(5):723-37 [PMID: 19453445]
  8. Fungal Genet Biol. 2009 Sep;46(9):667-81 [PMID: 19520179]
  9. Mol Plant Pathol. 2005 Nov 1;6(6):605-13 [PMID: 20565683]
  10. Mol Biol Evol. 2011 Oct;28(10):2731-9 [PMID: 21546353]
  11. Chem Rev. 2006 Aug;106(8):3468-96 [PMID: 16895337]
  12. Plant Cell. 2000 Sep;12(9):1703-18 [PMID: 11006342]
  13. Mol Microbiol. 2006 Aug;61(4):1069-80 [PMID: 16879655]
  14. Nucleic Acids Res. 2001 May 1;29(9):e45 [PMID: 11328886]
  15. Annu Rev Biochem. 1999;68:219-53 [PMID: 10872449]
  16. Mol Plant Microbe Interact. 2006 Feb;19(2):139-49 [PMID: 16529376]
  17. Mol Microbiol. 2007 Apr;64(2):293-307 [PMID: 17378924]
  18. Structure. 1997 Jul 15;5(7):907-20 [PMID: 9261083]
  19. Biosci Biotechnol Biochem. 1998;62(1):173-4 [PMID: 27393365]
  20. Mol Plant Pathol. 2012 May;13(4):414-30 [PMID: 22471698]
  21. Chem Biol. 2001 Feb;8(2):189-97 [PMID: 11251292]
  22. Mycol Res. 2008 Feb;112(Pt 2):207-15 [PMID: 18272356]
  23. Mol Plant Pathol. 2001 Jul 1;2(4):229-39 [PMID: 20573011]
  24. Fungal Genet Biol. 2003 Mar;38(2):143-58 [PMID: 12620252]
  25. Fungal Biol. 2015 Jul;119(7):580-94 [PMID: 26058534]
  26. PLoS Pathog. 2012;8(8):e1002888 [PMID: 22927822]
  27. Biosci Biotechnol Biochem. 2010;74(11):2220-5 [PMID: 21071840]
  28. Mol Plant Pathol. 2007 Mar;8(2):163-72 [PMID: 20507488]
  29. J Plant Physiol. 2011 Jan 1;168(1):51-62 [PMID: 20674079]
  30. Bioinformatics. 2007 Nov 1;23(21):2947-8 [PMID: 17846036]

MeSH Term

Benzaldehydes
Fatty Alcohols
Gene Expression Regulation, Fungal
Magnaporthe
Multigene Family
Oryza
Plant Diseases
Plant Leaves
Polyketide Synthases
Polyketides
Secondary Metabolism
Transcription Factors

Chemicals

Benzaldehydes
Fatty Alcohols
Polyketides
Transcription Factors
pyriculol
Polyketide Synthases

Word Cloud

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