A linear nonribosomal octapeptide from Fusarium graminearum facilitates cell-to-cell invasion of wheat.

Lei-Jie Jia, Hao-Yu Tang, Wan-Qiu Wang, Ting-Lu Yuan, Wan-Qian Wei, Bo Pang, Xue-Min Gong, Shou-Feng Wang, Yu-Jie Li, Dong Zhang, Wen Liu, Wei-Hua Tang
Author Information
  1. Lei-Jie Jia: National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, 200032, Shanghai, China.
  2. Hao-Yu Tang: State Key Laboratory of Bioorganic and Natural Products Chemistry, Center for Excellence in Molecular Synthesis, Shanghai Institute of Organic Chemistry, Chinese Academy of Sciences, 345 Lingling Road, 200032, Shanghai, China. ORCID
  3. Wan-Qiu Wang: National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, 200032, Shanghai, China.
  4. Ting-Lu Yuan: National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, 200032, Shanghai, China.
  5. Wan-Qian Wei: National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, 200032, Shanghai, China.
  6. Bo Pang: State Key Laboratory of Bioorganic and Natural Products Chemistry, Center for Excellence in Molecular Synthesis, Shanghai Institute of Organic Chemistry, Chinese Academy of Sciences, 345 Lingling Road, 200032, Shanghai, China.
  7. Xue-Min Gong: University of the Chinese Academy of Sciences, 200032, Shanghai, China.
  8. Shou-Feng Wang: State Key Laboratory of Bioorganic and Natural Products Chemistry, Center for Excellence in Molecular Synthesis, Shanghai Institute of Organic Chemistry, Chinese Academy of Sciences, 345 Lingling Road, 200032, Shanghai, China.
  9. Yu-Jie Li: National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, 200032, Shanghai, China.
  10. Dong Zhang: National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, 200032, Shanghai, China.
  11. Wen Liu: State Key Laboratory of Bioorganic and Natural Products Chemistry, Center for Excellence in Molecular Synthesis, Shanghai Institute of Organic Chemistry, Chinese Academy of Sciences, 345 Lingling Road, 200032, Shanghai, China. wliu@sioc.ac.cn.
  12. Wei-Hua Tang: National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, 300 Fenglin Road, 200032, Shanghai, China. whtang@sibs.ac.cn. ORCID

Abstract

Fusarium graminearum is a destructive wheat pathogen. No fully resistant cultivars are available. Knowledge concerning the molecular weapons of F. graminearum to achieve infection remains limited. Here, we report that deletion of the putative secondary metabolite biosynthesis gene cluster fg3_54 compromises the pathogen's ability to infect wheat through cell-to-cell penetration. Ectopic expression of fgm4, a pathway-specific bANK-like regulatory gene, activates the transcription of the fg3_54 cluster in vitro. We identify a linear, C- terminally reduced and D-amino acid residue-rich octapeptide, fusaoctaxin A, as the product of the two nonribosomal peptide synthetases encoded by fg3_54. Chemically-synthesized fusaoctaxin A restores cell-to-cell invasiveness in fg3_54-deleted F. graminearum, and enables colonization of wheat coleoptiles by two Fusarium strains that lack the fg3_54 homolog and are nonpathogenic to wheat. In conclusion, our results identify fusaoctaxin A as a virulence factor required for cell-to-cell invasion of wheat by F. graminearum.

References

  1. JAMA. 2006 Aug 23;296(8):953-63 [PMID: 16926355]
  2. BMC Genomics. 2013 Mar 21;14:197 [PMID: 23514540]
  3. Annu Rev Microbiol. 2013;67:399-416 [PMID: 24024636]
  4. Fungal Genet Biol. 2008 Apr;45(4):389-99 [PMID: 17950638]
  5. Angew Chem Int Ed Engl. 2003 Feb 17;42(7):730-65 [PMID: 12596194]
  6. Trends Pharmacol Sci. 2017 Apr;38(4):406-424 [PMID: 28209404]
  7. Mol Plant Pathol. 2004 Nov 1;5(6):515-25 [PMID: 20565626]
  8. Environ Microbiol. 2015 Nov;17(11):4580-99 [PMID: 26177389]
  9. Mol Plant Microbe Interact. 2009 Aug;22(8):899-908 [PMID: 19589066]
  10. Plant Cell. 2012 Dec;24(12):5159-76 [PMID: 23266949]
  11. BMC Genomics. 2012 Oct 04;13:525 [PMID: 23033934]
  12. Nat Protoc. 2016 Sep;11(9):1650-67 [PMID: 27560171]
  13. EMBO J. 1990 Mar;9(3):741-7 [PMID: 2107074]
  14. Plant Cell. 1995 Nov;7(11):1941-50 [PMID: 8535144]
  15. Mol Plant Pathol. 2008 Jul;9(4):435-45 [PMID: 18705859]
  16. Mol Plant Microbe Interact. 2011 Sep;24(9):995-1000 [PMID: 21585270]
  17. Nat Prod Rep. 2012 Oct;29(10):1074-98 [PMID: 22802156]
  18. Fungal Genet Biol. 2006 May;43(5):316-25 [PMID: 16531083]
  19. PLoS Pathog. 2011 Oct;7(10):e1002310 [PMID: 22028654]
  20. Science. 2007 Sep 7;317(5843):1400-2 [PMID: 17823352]
  21. PLoS One. 2010 Dec 07;5(12):e15319 [PMID: 21151869]
  22. Fungal Genet Biol. 2015 Feb;75:20-9 [PMID: 25543026]
  23. Chem Biol. 1999 Aug;6(8):493-505 [PMID: 10421756]
  24. PLoS One. 2013 Nov 11;8(11):e79042 [PMID: 24244413]
  25. Nucleic Acids Res. 2015 Jan;43(Database issue):D645-55 [PMID: 25414340]
  26. Science. 2018 Mar 23;359(6382):1399-1403 [PMID: 29567712]
  27. Plant J. 2005 May;42(3):364-75 [PMID: 15842622]
  28. PLoS Pathog. 2011 Dec;7(12):e1002460 [PMID: 22216007]
  29. Nat Commun. 2017 Feb 06;8:14318 [PMID: 28165456]
  30. Proc Natl Acad Sci U S A. 2012 Jan 24;109(4):1287-92 [PMID: 22232661]
  31. Nat Chem Biol. 2009 Jul;5(7):450-2 [PMID: 19536102]
  32. J Agric Food Chem. 2007 Jun 27;55(13):5186-93 [PMID: 17547419]
  33. Plant Cell. 2009 Feb;21(2):581-94 [PMID: 19223515]
  34. Chem Sci. 2015 Aug 1;6(8):4837-4845 [PMID: 29142718]
  35. Plant Physiol. 2014 May;165(1):346-58 [PMID: 24686113]
  36. Nat Biotechnol. 2015 Mar;33(3):290-5 [PMID: 25690850]
  37. Mol Microbiol. 2005 Nov;58(4):1102-13 [PMID: 16262793]
  38. Methods Mol Biol. 2015;1217:149-56 [PMID: 25287202]
  39. Essays Biochem. 2015;58:115-31 [PMID: 26374891]
  40. Proc Natl Acad Sci U S A. 2005 Nov 15;102(46):16892-7 [PMID: 16263921]
  41. Mol Plant Pathol. 2018 Jun;19(6):1523-1536 [PMID: 29045052]
  42. BMC Mol Biol. 2009 Feb 20;10:11 [PMID: 19232096]
  43. New Phytol. 2014 Nov;204(3):650-60 [PMID: 25138067]
  44. Front Microbiol. 2015 Jan 12;5:759 [PMID: 25628608]
  45. Toxicol Lett. 2013 Feb 27;217(2):149-58 [PMID: 23274714]
  46. Chem Rev. 2005 Feb;105(2):715-38 [PMID: 15700962]
  47. Genome Res. 2004 Jul;14(7):1394-403 [PMID: 15231754]
  48. Nat Commun. 2012 Jun 26;3:926 [PMID: 22735454]
  49. PLoS One. 2013 Jul 16;8(7):e68441 [PMID: 23874628]
  50. Nat Methods. 2015 Apr;12(4):357-60 [PMID: 25751142]
  51. Mol Plant Microbe Interact. 1995 Jul-Aug;8(4):593-601 [PMID: 8589414]
  52. Annu Rev Phytopathol. 2004;42:135-61 [PMID: 15283663]
  53. PLoS Pathog. 2016 Mar 14;12(3):e1005485 [PMID: 26974960]
  54. Plant Cell. 1999 Feb;11(2):237-49 [PMID: 9927641]
  55. Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):14174-9 [PMID: 11698648]
  56. PLoS Biol. 2018 May 3;16(5):e2004122 [PMID: 29723186]
  57. Nat Microbiol. 2016 Apr 11;1(6):16043 [PMID: 27572834]
  58. Microbiol Rev. 1993 Sep;57(3):595-604 [PMID: 8246841]
  59. PLoS One. 2014 Oct 15;9(10):e110311 [PMID: 25333987]
  60. New Phytol. 2018 Jan;217(1):62-67 [PMID: 29083038]
  61. J Antibiot (Tokyo). 1970 May;23(5):259-62 [PMID: 4912600]
  62. New Phytol. 2015 Jul;207(1):119-34 [PMID: 25758923]
  63. Mol Plant Microbe Interact. 2001 Mar;14(3):336-48 [PMID: 11277431]
  64. Mol Plant Pathol. 2006 Nov;7(6):449-61 [PMID: 20507460]
  65. Angew Chem Int Ed Engl. 2017 Mar 27;56(14):3770-3821 [PMID: 28323366]
  66. Nat Plants. 2015 Jun 01;1:15074 [PMID: 27250009]
  67. Brief Bioinform. 2013 Mar;14(2):178-92 [PMID: 22517427]
  68. Fungal Genet Biol. 2005 May;42(5):420-33 [PMID: 15809006]
  69. Plant Cell. 2006 Oct;18(10):2836-53 [PMID: 17056706]
  70. Chembiochem. 2004 Sep 6;5(9):1196-1203 [PMID: 15368570]
  71. Nat Genet. 2016 Dec;48(12):1576-1580 [PMID: 27776114]
  72. PLoS One. 2014 Nov 19;9(11):e112703 [PMID: 25409087]
  73. J Nat Prod. 2014 Dec 26;77(12):2619-25 [PMID: 25412204]
  74. Plant Cell. 2004 Sep;16(9):2499-513 [PMID: 15319478]

MeSH Term

Cotyledon
Fungal Proteins
Fusarium
Oligopeptides
Peptide Synthases
Plant Diseases
Triticum
Virulence

Chemicals

Fungal Proteins
Oligopeptides
Peptide Synthases
non-ribosomal peptide synthase