Heterochromatin influences the secondary metabolite profile in the plant pathogen Fusarium graminearum

Fungal Genetics and Biology

Volumn 49, Issue 1, 2012, Pages 39-47

  Reyes Dominguez, Yazmid ^a   Boedi, Stefan ^a   Sulyok, Michael ^c   Wiesenberger, Gerlinde ^a   Stoppacher, Norbert ^c   Krska, Rudolf ^c   Strauss, Joseph ^a,b  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b AIT AUSTRIAN INSTITUTE OF TECHNOLOGY   (Austria)

^c UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

Aurofusarin; Deoxynivalenol; Fusarium graminearum; Heterochromatin protein; Mycotoxins; Secondary metabolism

Indexed keywords

ARTICLE; AUR GENE; BIOSYNTHESIS; CONTROLLED STUDY; FUNGAL GENE; FUSARIUM GRAMINEARUM; GENE CLUSTER; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; HEP1 GENE; HETEROCHROMATIN; NONHUMAN; OPEN READING FRAME; PLANT GROWTH; PRIORITY JOURNAL; UPREGULATION;

FUNGAL PROTEINS; FUSARIUM; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; HETEROCHROMATIN; HISTONES; NAPHTHOQUINONES; TRICHOTHECENES;

EMERICELLA NIDULANS; FUNGI; GIBBERELLA ZEAE;

EID: 84856432508     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2011.11.002     Document Type: Article

References (71)

1. Aagaard L., Laible G., Selenko P., Schmid M., Dorn R., Schotta G., Kuhfittig S., Wolf A., Lebersorger A., Singh P.B., Reuter G., Jenuwein T. Functional mammalian homologues of the Drosophila PEV-modifier Su(var)3-9 encode centromere-associated proteins which complex with the heterochromatin component M31. EMBO J. 1999, 18:1923-1938.
2. Aasland R., Stewart A.F. The chromo shadow domain, a second chromo domain in heterochromatin-binding protein 1, HP1. Nucleic Acids Res. 1995, 23:3168-3173.
3. Allshire R.C. Elements of chromosome structure and function in fission yeast. Semin. Cell Biol. 1995, 6:55-64.
4. Allshire R.C., Karpen G.H. Epigenetic regulation of centromeric chromatin: old dogs, new tricks?. Nat. Rev. Genet. 2008, 9:923-937.
5. Ausubel F., Moore D., Brent R., Seidman J.G. Current Protocols in Molecular Biology 1998, Wiley, John & Sons.
6. Ayoub N., Jeyasekharan A.D., Venkitaraman A.R. Mobilization and recruitment of HP1: a bimodal response to DNA breakage. Cell Cycle 2009, 8:2945-2950.
7. Ball A.R., Yokomori K. Revisiting the role of heterochromatin protein 1 in DNA repair. J. Cell Biol. 2009, 185:573-575.
8. Bayram O., Krappmann S., Ni M., Bok J.W., Helmstaedt K., Valerius O., Braus-Stromeyer S., Kwon N.J., Keller N.P., Yu J.H., Braus G.H. VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 2008, 320:1504-1506.
9. Bergmann S., Schumann J., Scherlach K., Lange C., Brakhage A.A., Hertweck C. Genomics-driven discovery of PKS-NRPS hybrid metabolites from Aspergillus nidulans. Nat. Chem. Biol. 2007, 3:213-217.
10. Bernreiter A., Ramon A., Fernandez-Martinez J., Berger H., Araujo-Bazan L., Espeso E.A., Pachlinger R., Gallmetzer A., Anderl I., Scazzocchio C., Strauss J. Nuclear export of the transcription factor NirA is a regulatory checkpoint for nitrate induction in Aspergillus nidulans. Mol. Cell. Biol. 2007, 27:791-802.
11. Bohnert M., Wackler B., Hoffmeister D. Spotlights on advances in mycotoxin research. Appl. Microbiol. Biotechnol. 2010, 87:1-7.
12. Bok J.W., Keller N.P. LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot. Cell 2004, 3:527-535.
13. Bok J.W., Chiang Y.M., Szewczyk E., Reyes-Dominguez Y., Davidson A.D., Sanchez J.F., Lo H.C., Watanabe K., Strauss J., Oakley B.R., Wang C.C., Keller N.P. Chromatin-level regulation of biosynthetic gene clusters. Nat. Chem. Biol. 2009, 5:462-464.
14. Cheung P., Lau P. Epigenetic regulation by histone methylation and histone variants. Mol. Endocrinol. 2005, 19:563-573.
15. Cryderman D.E., Grade S.K., Li Y., Fanti L., Pimpinelli S., Wallrath L.L. Role of Drosophila HP1 in euchromatic gene expression. Dev. Dyn. 2005, 232:767-774.
16. Cuomo C.A., Guldener U., Xu J.R., Trail F., Turgeon B.G., Di Pietro A., Walton J.D., Ma L.J., Baker S.E., Rep M., Adam G., Antoniw J., Baldwin T., Calvo S., Chang Y.L., Decaprio D., Gale L.R., Gnerre S., Goswami R.S., Hammond-Kosack K., Harris L.J., Hilburn K., Kennell J.C., Kroken S., Magnuson J.K., Mannhaupt G., Mauceli E., Mewes H.W., Mitterbauer R., Muehlbauer G., Munsterkotter M., Nelson D., O'Donnell K., Ouellet T., Qi W., Quesneville H., Roncero M.I., Seong K.Y., Tetko I.V., Urban M., Waalwijk C., Ward T.J., Yao J., Birren B.W., Kistler H.C. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 2007, 317:1400-1402.
17. Desjardins A.E., Proctor R.H. Molecular biology of Fusarium mycotoxins. Int. J. Food Microbiol. 2007, 119:47-50.
18. Desjardins A.E., Hohn T.M., McCormick S.P. Trichothecene biosynthesis in Fusarium species: chemistry, genetics, and significance. Microbiol. Rev. 1993, 57:595-604.
19. D'Mello, Placinta, Macdonald Fusarium mycotoxins: a review of global implications for animal health, welfare and productivity. Animal Feed Science and Technology 1999, 80:183-205.
20. Ekwall K., Nimmo E.R., Javerzat J.P., Borgstrom B., Egel R., Cranston G., Allshire R. Mutations in the fission yeast silencing factors clr4+ and rik1+ disrupt the localisation of the chromo domain protein Swi6p and impair centromere function. J. Cell Sci. 1996, 109(Pt 11):2637-2648.
21. Elgin S.C., Grewal S.I. Heterochromatin: silence is golden. Curr. Biol. 2003, 13:R895-898.
22. Fanti L., Giovinazzo G., Berloco M., Pimpinelli S. The heterochromatin protein 1 prevents telomere fusions in Drosophila. Mol. Cell 1998, 2:527-538.
23. Frandsen R.J., Nielsen N.J., Maolanon N., Sorensen J.C., Olsson S., Nielsen J., Giese H. The biosynthetic pathway for aurofusarin in Fusarium graminearum reveals a close link between the naphthoquinones and naphthopyrones. Mol. Microbiol. 2006, 61:1069-1080.
24. Freitag M., Hickey P.C., Khlafallah T.K., Read N.D., Selker E.U. HP1 is essential for DNA methylation in Neurospora. Mol. Cell 2004, 13:427-434.
25. Gaffoor I., Brown D.W., Plattner R., Proctor R.H., Qi W., Trail F. Functional analysis of the polyketide synthase genes in the filamentous fungus Gibberella zeae (anamorph Fusarium graminearum). Eukaryot. Cell 2005, 4:1926-1933.
26. Gardiner D.M., Kazan K., Manners J.M. Novel genes of Fusarium graminearum that negatively regulate deoxynivalenol production and virulence. Mol. Plant Microbe Interact. 2009, 22:1588-1600.
27. Grewal S.I., Elgin S.C. Heterochromatin: new possibilities for the inheritance of structure. Curr. Opin. Genet. Dev. 2002, 12:178-187.
28. Guldener U., Mannhaupt G., Munsterkotter M., Haase D., Oesterheld M., Stumpflen V., Mewes H.W., Adam G. FGDB: a comprehensive fungal genome resource on the plant pathogen Fusarium graminearum. Nucleic Acids Res. 2006, 34:D456-458.
29. Hediger F., Gasser S.M. Heterochromatin protein 1: don't judge the book by its cover!. Curr. Opin. Genet. Dev. 2006, 16:143-150.
30. Hohn T.M., Krishna R., Proctor R.H. Characterization of a transcriptional activator controlling trichothecene toxin biosynthesis. Fungal Genet. Biol. 1999, 26:224-235.
31. Honda S., Selker E.U. Direct interaction between DNA methyltransferase DIM-2 and HP1 is required for DNA methylation in Neurospora crassa. Mol. Cell. Biol. 2008, 28:6044-6055.
32. Jurgenson J.E., Bowden R.L., Zeller K.A., Leslie J.F., Alexander N.J., Plattner R.D. A genetic map of Gibberella zeae (Fusarium graminearum). Genetics 2002, 160:1451-1460.
33. Keller N.P., Hohn T.M. Metabolic pathway gene clusters in filamentous fungi. Fungal Genet. Biol. 1997, 21:17-29.
34. Keller N.P., Turner G., Bennett J.W. Fungal secondary metabolism - from biochemistry to genomics. Nat. Rev. Microbiol. 2005, 3:937-947.
35. Kim J.E., Han K.H., Jin J., Kim H., Kim J.C., Yun S.H., Lee Y.W. Putative polyketide synthase and laccase genes for biosynthesis of aurofusarin in Gibberella zeae. Appl. Environ. Microbiol. 2005, 71:1701-1708.
36. Kimura M., Tokai T., O'Donnell K., Ward T.J., Fujimura M., Hamamoto H., Shibata T., Yamaguchi I. The trichothecene biosynthesis gene cluster of Fusarium graminearum F15 contains a limited number of essential pathway genes and expressed non-essential genes. FEBS Lett. 2003, 539:105-110.
37. Kimura M., Tokai T., Takahashi-Ando N., Ohsato S., Fujimura M. Molecular and genetic studies of Fusarium trichothecene biosynthesis: pathways, genes, and evolution. Biosci. Biotechnol. Biochem. 2007, 71:2105-2123.
38. Kwon S.H., Workman J.L. The heterochromatin protein 1 (HP1) family: put away a bias toward HP1. Mol. Cells 2008, 26:217-227.
39. Kwon S.H., Workman J.L. The changing faces of HP1: from heterochromatin formation and gene silencing to euchromatic gene expression: HP1 acts as a positive regulator of transcription. BioEssays 2011, 33:280-289.
40. Lachner M., O'Carroll D., Rea S., Mechtler K., Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 2001, 410:116-120.
41. Lemmens M., Scholz U., Berthiller F., Dall'Asta C., Koutnik A., Schuhmacher R., Adam G., Buerstmayr H., Mesterhazy A., Krska R., Ruckenbauer P. The ability to detoxify the mycotoxin deoxynivalenol colocalizes with a major quantitative trait locus for Fusarium head blight resistance in wheat. Mol. Plant Microbe Interact. 2005, 18:1318-1324.
42. Leonard K., Bushnell W. Fusarium Head Blight of Wheat and Barley 2003, APS Press, St. Paul, MN.
43. Lewis Z.A., Adhvaryu K.K., Honda S., Shiver A.L., Selker E.U. Identification of DIM-7, a protein required to target the DIM-5 H3 methyltransferase to chromatin. Proc. Natl. Acad. Sci. USA 2010, 107:8310-8315.
44. Li Y., Kirschmann D.A., Wallrath L.L. Does heterochromatin protein 1 always follow code?. Proc. Natl. Acad. Sci. USA 2002, 99(Suppl. 4):16462-16469.
45. Lomberk G., Wallrath L., Urrutia R. The heterochromatin protein 1 family. Genome Biol. 2006, 7:228.
46. Lu B.Y., Emtage P.C., Duyf B.J., Hilliker A.J., Eissenberg J.C. Heterochromatin protein 1 is required for the normal expression of two heterochromatin genes in Drosophila. Genetics 2000, 155:699-708.
47. Mach R.L., Schindler M., Kubicek C.P. Transformation of Trichoderma reesei based on hygromycin B resistance using homologous expression signals. Curr. Genet. 1994, 25:567-570.
48. Maison C., Almouzni G. HP1 and the dynamics of heterochromatin maintenance. Nat. Rev. Mol. Cell Biol. 2004, 5:296-304.
49. Malz S., Grell M.N., Thrane C., Maier F.J., Rosager P., Felk A., Albertsen K.S., Salomon S., Bohn L., Schafer W., Giese H. Identification of a gene cluster responsible for the biosynthesis of aurofusarin in the Fusarium graminearum species complex. Fungal Genet. Biol. 2005, 42:420-433.
50. McMullen M., Jones R., Gallenberg D. Scab of wheat and barley: a re-emerging disease of devastating impact. Plant Dis. 1997, 81:1340-1348.
51. Meek I.B., Peplow A.W., Ake C., Phillips T.D., Beremand M.N. Tri1 encodes the cytochrome P450 monooxygenase for C-8 hydroxylation during trichothecene biosynthesis in Fusarium sporotrichioides and resides upstream of another new Tri gene. Appl. Environ. Microbiol. 2003, 69:1607-1613.
52. Nielsen P.R., Nietlispach D., Mott H.R., Callaghan J., Bannister A., Kouzarides T., Murzin A.G., Murzina N.V., Laue E.D. Structure of the HP1 chromodomain bound to histone H3 methylated at lysine 9. Nature 2002, 416:103-107.
53. Norwood L.E., Grade S.K., Cryderman D.E., Hines K.A., Furiasse N., Toro R., Li Y., Dhasarathy A., Kladde M.P., Hendrix M.J., Kirschmann D.A., Wallrath L.L. Conserved properties of HP1 (Hsalpha). Gene 2004, 336:37-46.
54. Paterson R.R., Lima N. Toxicology of mycotoxins. EXS 2010, 100:31-63.
55. Perrini B., Piacentini L., Fanti L., Altieri F., Chichiarelli S., Berloco M., Turano C., Ferraro A., Pimpinelli S. HP1 controls telomere capping, telomere elongation, and telomere silencing by two different mechanisms in Drosophila. Mol. Cell 2004, 15:467-476.
56. Piacentini L., Fanti L., Negri R., Del Vescovo V., Fatica A., Altieri F., Pimpinelli S. Heterochromatin protein 1 (HP1a) positively regulates euchromatic gene expression through RNA transcript association and interaction with hnRNPs in Drosophila. PLoS Genet. 2009, 5:e1000670.
57. Proctor R.H., Hohn T.M., McCormick S.P. Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol. Plant Microbe Interact. 1995, 8:593-601.
58. Proctor R.H., Hohn T.M., McCormick S.P., Desjardins A.E. Tri6 encodes an unusual zinc finger protein involved in regulation of trichothecene biosynthesis in Fusarium sporotrichioides. Appl. Environ. Microbiol. 1995, 61:1923-1930.
59. Reyes-Dominguez Y., Bok J.W., Berger H., Shwab E.K., Basheer A., Gallmetzer A., Scazzocchio C., Keller N., Strauss J. Heterochromatic marks are associated with the repression of secondary metabolism clusters in Aspergillus nidulans. Mol. Microbiol. 2010, 76:1376-1386.
60. Richards E.J., Elgin S.C. Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 2002, 108:489-500.
61. Rountree M.R., Selker E.U. DNA methylation and the formation of heterochromatin in Neurospora crassa. Heredity 2010, 105:38-44.
62. Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA.
63. Schotta G., Ebert A., Krauss V., Fischer A., Hoffmann J., Rea S., Jenuwein T., Dorn R., Reuter G. Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J. 2002, 21:1121-1131.
64. Schroeckh V., Scherlach K., Nutzmann H.W., Shelest E., Schmidt-Heck W., Schuemann J., Martin K., Hertweck C., Brakhage A.A. Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 2009, 106:14558-14563.
65. Shaffer C.D., Wallrath L.L., Elgin S.C. Regulating genes by packaging domains: bits of heterochromatin in euchromatin?. Trends Genet. 1993, 9:35-37.
66. Smith K.M., Phatale P.A., Sullivan C.M., Pomraning K.R., Freitag M. Heterochromatin is required for normal distribution of Neurospora CenH3. Mol. Cell. Biol 2011.
67. Tamaru H., Zhang X., McMillen D., Singh P.B., Nakayama J., Grewal S.I., Allis C.D., Cheng X., Selker E.U. Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat. Genet. 2003, 34:75-79.
68. Vishwanath V., Sulyok M., Labuda R., Bicker W., Krska R. Simultaneous determination of 186 fungal and bacterial metabolites in indoor matrices by liquid chromatography/tandem mass spectrometry. Anal. Bioanal. Chem. 2009, 395:1355-1372.
69. Wiemann P., Brown D.W., Kleigrewe K., Bok J.W., Keller N.P., Humpf H.U., Tudzynski B. FfVel1 and FfLae1, components of a velvet-like complex in Fusarium fujikuroi, affect differentiation, secondary metabolism and virulence. Mol. Microbiol. 2010, 77:972-994.
70. Wu Q., Dohnal V., Huang L., Kuca K., Yuan Z. Metabolic pathways of trichothecenes. Drug Metab. Rev. 2010, 42:250-267.
71. Yu J.H., Keller N. Regulation of secondary metabolism in filamentous fungi. Annu. Rev. Phytopathol. 2005, 43:437-458.