1887

Abstract

The velvet genes are conserved in ascomycetous fungi and function as global regulators of differentiation and secondary metabolism. Here, we characterized one of the velvet genes, designated , in the plant-pathogenic fungus , which causes fusarium head blight in cereals and produces mycotoxins within plants. -deleted (Δ) strains produced fewer aerial mycelia with less pigmentation than those of the wild-type (WT) during vegetative growth. Under sexual development conditions, the Δ strains produced no fruiting bodies but retained male fertility, and conidiation was threefold higher compared with the WT strain. Production of trichothecene and zearalenone was dramatically reduced compared with the WT strain. In addition, the Δ strains were incapable of colonizing host plant tissues. Transcript analyses revealed that was highly expressed during the sexual development stage, and may be regulated by a mitogen-activated protein kinase cascade. Microarray analysis showed that affects regulatory pathways mediated by the mating-type loci and a G-protein alpha subunit, as well as primary and secondary metabolism. These results suggest that FgVelB has diverse biological functions, probably by acting as a member of a possible velvet protein complex, although identification of the FgVelB–FgVeA complex and the determination of its roles require further investigation.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.059188-0
2012-07-01
2020-08-12
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/7/1723.html?itemId=/content/journal/micro/10.1099/mic.0.059188-0&mimeType=html&fmt=ahah

References

  1. Bayram Ö., Braus G. H.. ( 2012;). Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol Rev36:1–24 [CrossRef][PubMed]
    [Google Scholar]
  2. Bayram Ö., Krappmann S., Ni M., Bok J. W., Helmstaedt K., Valerius O., Braus-Stromeyer S., Kwon N.-J., Keller N. P. et al. ( 2008;). VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science320:1504–1506 [CrossRef][PubMed]
    [Google Scholar]
  3. Bayram O., Bayram Ö., Valerius O., Park H. S., Irniger S., Gerke J., Ni M., Han K.-H., Yu J.-H., Braus G. H.. ( 2010;). LaeA control of velvet family regulatory proteins for light-dependent development and fungal cell-type specificity. PLoS Genet6:e1001226 [CrossRef][PubMed]
    [Google Scholar]
  4. Bok J. W., Noordermeer D., Kale S. P., Keller N. P.. ( 2006;). Secondary metabolic gene cluster silencing in Aspergillus nidulans. Mol Microbiol61:1636–1645 [CrossRef][PubMed]
    [Google Scholar]
  5. Bowden R. L., Fuentes-Bueno I., Leslie J. F., Lee J., Lee Y.-W.. ( 2008;). Methods for detecting chromosome rearrangements in Gibberella zeae. Cereal Res Commun36:Suppl. 6603–608 [CrossRef]
    [Google Scholar]
  6. Desjardins A. E.. ( 2006;). Fusarium Mycotoxin: Chemistry, Genetics and Biology St Paul, MN: APS Press;
    [Google Scholar]
  7. Han Y.-K., Kim M.-D., Lee S.-H., Yun S.-H., Lee Y.-W.. ( 2007;). A novel F-box protein involved in sexual development and pathogenesis in Gibberella zeae. Mol Microbiol63:768–779 [CrossRef][PubMed]
    [Google Scholar]
  8. Harris L. J., Alexander N. J., Saparno A., Blackwell B., McCormick S. P., Desjardins A. E., Robert L. S., Tinker N., Hattori J. et al. ( 2007;). A novel gene cluster in Fusarium graminearum contains a gene that contributes to butenolide synthesis. Fungal Genet Biol44:293–306 [CrossRef][PubMed]
    [Google Scholar]
  9. Hong S. Y., So J., Lee J., Min K., Son H., Park C., Yun S.-H., Lee Y.-W.. ( 2010;). Functional analyses of two syntaxin-like SNARE genes, GzSYN1 and GzSYN2, in the ascomycete Gibberella zeae. Fungal Genet Biol47:364–372 [CrossRef][PubMed]
    [Google Scholar]
  10. Hou Z., Xue C., Peng Y., Katan T., Kistler H. C., Xu J. R.. ( 2002;). A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol Plant Microbe Interact15:1119–1127 [CrossRef][PubMed]
    [Google Scholar]
  11. Jenczmionka N. J., Maier F. J., Lösch A. P., Schäfer W.. ( 2003;). Mating, conidiation and pathogenicity of Fusarium graminearum, the main causal agent of the head-blight disease of wheat, are regulated by the MAP kinase gpmk1. Curr Genet43:87–95[PubMed]
    [Google Scholar]
  12. Jiang J., Liu X., Yin Y., Ma Z.. ( 2011;). Involvement of a velvet protein FgVeA in the regulation of asexual development, lipid and secondary metabolisms and virulence in Fusarium graminearum. PLoS ONE6:e28291 [CrossRef][PubMed]
    [Google Scholar]
  13. Kanehisa M., Goto S., Hattori M., Aoki-Kinoshita K. F., Itoh M., Kawashima S., Katayama T., Araki M., Hirakawa M.. ( 2006;). From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res34:Database issueD354–D357 [CrossRef][PubMed]
    [Google Scholar]
  14. Kato N., Brooks W., Calvo A. M.. ( 2003;). The expression of sterigmatocystin and penicillin genes in Aspergillus nidulans is controlled by veA, a gene required for sexual development. Eukaryot Cell2:1178–1186 [CrossRef][PubMed]
    [Google Scholar]
  15. Keller N. P., Turner G., Bennett J. W.. ( 2005;). Fungal secondary metabolism – from biochemistry to genomics. Nat Rev Microbiol3:937–947 [CrossRef][PubMed]
    [Google Scholar]
  16. Kim H.-K., Yun S.-H.. ( 2011;). Evaluation of potential reference genes for quantitative RT-PCR analysis in Fusarium graminearum under different culture conditions. Plant Pathol J27:301–309 [CrossRef]
    [Google Scholar]
  17. Kim H.-S., Han K. Y., Kim K.-J., Han D.-M., Jahng K.-Y., Chae K.-S.. ( 2002;). The veA gene activates sexual development in Aspergillus nidulans. Fungal Genet Biol37:72–80 [CrossRef][PubMed]
    [Google Scholar]
  18. Kim J.-E., Han K.-H., Jin J., Kim H., Kim J.-C., Yun S.-H., Lee Y. W.. ( 2005a;). Putative polyketide synthase and laccase genes for biosynthesis of aurofusarin in Gibberella zeae. Appl Environ Microbiol71:1701–1708 [CrossRef][PubMed]
    [Google Scholar]
  19. Kim Y.-T., Lee Y.-R., Jin J., Han K.-H., Kim H., Kim J.-C., Lee T., Yun S.-H., Lee Y.-W.. ( 2005b;). Two different polyketide synthase genes are required for synthesis of zearalenone in Gibberella zeae. Mol Microbiol58:1102–1113 [CrossRef][PubMed]
    [Google Scholar]
  20. Kim J.-E., Jin J., Kim H., Kim J. C., Yun S. H., Lee Y. W.. ( 2006;). GIP2, a putative transcription factor that regulates the aurofusarin biosynthetic gene cluster in Gibberella zeae. Appl Environ Microbiol72:1645–1652 [CrossRef][PubMed]
    [Google Scholar]
  21. Kim H.-K., Lee T., Yun S.-H.. ( 2008;). A putative pheromone signaling pathway is dispensable for self-fertility in the homothallic ascomycete Gibberella zeae. Fungal Genet Biol45:1188–1196 [CrossRef][PubMed]
    [Google Scholar]
  22. Kim J.-E., Lee H.-J., Lee J., Kim K. W., Yun S.-H., Shim W.-B., Lee Y.-W.. ( 2009;). Gibberella zeae chitin synthase genes, GzCHS5 and GzCHS7, are required for hyphal growth, perithecia formation, and pathogenicity. Curr Genet55:449–459 [CrossRef][PubMed]
    [Google Scholar]
  23. Kim H.-K., Lee Y.-W., Yun S.-H.. ( 2011;). GzRUM1, encoding an ortholog of human retinoblastoma binding protein 2, is required for ascospore development in Gibberella zeae. Plant Pathol J27:20–25 [CrossRef]
    [Google Scholar]
  24. Kroken S., Glass N. L., Taylor J. W., Yoder O. C., Turgeon B. G.. ( 2003;). Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc Natl Acad Sci U S A100:15670–15675 [CrossRef][PubMed]
    [Google Scholar]
  25. Lee T., Han Y.-K., Kim K.-H., Yun S.-H., Lee Y.-W.. ( 2002;). Tri13 and Tri7 determine deoxynivalenol- and nivalenol-producing chemotypes of Gibberella zeae. Appl Environ Microbiol68:2148–2154 [CrossRef][PubMed]
    [Google Scholar]
  26. Lee J., Lee T., Lee Y.-W., Yun S.-H., Turgeon B. G.. ( 2003;). Shifting fungal reproductive mode by manipulation of mating type genes: obligatory heterothallism of Gibberella zeae. Mol Microbiol50:145–152 [CrossRef][PubMed]
    [Google Scholar]
  27. Lee S.-H., Lee J., Lee S., Park E.-H., Kim K. W., Kim M.-D., Yun S.-H., Lee Y.-W.. ( 2009;). GzSNF1 is required for normal sexual and asexual development in the ascomycete Gibberella zeae. Eukaryot Cell8:116–127 [CrossRef][PubMed]
    [Google Scholar]
  28. Lee J., Park C., Kim J.-C., Kim J.-E., Lee Y.-W.. ( 2010;). Identification and functional characterization of genes involved in the sexual reproduction of the ascomycete fungus Gibberella zeae. Biochem Biophys Res Commun401:48–52 [CrossRef][PubMed]
    [Google Scholar]
  29. Lee S., Son H., Lee J., Min K., Choi G. J., Kim J.-C., Lee Y.-W.. ( 2011;). Functional analyses of two acetyl coenzyme A synthetases in the ascomycete Gibberella zeae. Eukaryot Cell10:1043–1052 [CrossRef][PubMed]
    [Google Scholar]
  30. Leslie J. F., Summerell B. A.. ( 2006;). The Fusarium Laboratory Manual Ames, IA: Blackwell Professional; [CrossRef]
    [Google Scholar]
  31. Merhej J., Urban M., Dufresne M., Hammond-Kosack K. E., Richard-Forget F., Barreau C.. ( 2012;). The velvet gene, FgVe1, affects fungal development and positively regulates trichothecene biosynthesis and pathogenicity in Fusarium graminearum. Mol Plant Pathol13:363–374 [CrossRef][PubMed]
    [Google Scholar]
  32. Namiki F., Matsunaga M., Okuda M., Inoue I., Nishi K., Fujita Y., Tsuge T.. ( 2001;). Mutation of an arginine biosynthesis gene causes reduced pathogenicity in Fusarium oxysporum f. sp. melonis. Mol Plant Microbe Interact14:580–584 [CrossRef][PubMed]
    [Google Scholar]
  33. O’Donnell K., Kistler H. C., Tacke B. K., Casper H. H.. ( 2000;). Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proc Natl Acad Sci U S A97:7905–7910 [CrossRef][PubMed]
    [Google Scholar]
  34. Oide S., Krasnoff S. B., Gibson D. M., Turgeon B. G.. ( 2007;). Intracellular siderophores are essential for ascomycete sexual development in heterothallic Cochliobolus heterostrophus and homothallic Gibberella zeae. Eukaryot Cell6:1339–1353 [CrossRef][PubMed]
    [Google Scholar]
  35. Oide S., Liu J., Yun S.-H., Wu D., Michev A., Choi M. Y., Horwitz B. A., Turgeon B. G.. ( 2010;). Histidine kinase two-component response regulator proteins regulate reproductive development, virulence, and stress responses of the fungal cereal pathogens Cochliobolus heterostrophus and Gibberella zeae. Eukaryot Cell9:1867–1880 [CrossRef][PubMed]
    [Google Scholar]
  36. Parry D. W., Jenkinson P., McLeod L.. ( 1995;). Fusarium ear blight (scab) in small grain cereals–a review. Plant Pathol44:207–238 [CrossRef]
    [Google Scholar]
  37. Proctor R. H., Hohn T. M., McCormick S. P.. ( 1995;). Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol Plant Microbe Interact8:593–601 [CrossRef][PubMed]
    [Google Scholar]
  38. Ramamoorthy V., Zhao X., Snyder A. K., Xu J. R., Shah D. M.. ( 2007;). Two mitogen-activated protein kinase signalling cascades mediate basal resistance to antifungal plant defensins in Fusarium graminearum. Cell Microbiol9:1491–1506 [CrossRef][PubMed]
    [Google Scholar]
  39. Sambrook J., Russell D. W.. ( 2001;). Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  40. Seo J.-A., Kim J.-C., Lee D.-H., Lee Y.-W.. ( 1996;). Variation in 8-ketotrichothecenes and zearalenone production by Fusarium graminearum isolates from corn and barley in Korea. Mycopathologia134:31–37 [CrossRef][PubMed]
    [Google Scholar]
  41. Son H., Lee J., Park A. R., Lee Y.-W.. ( 2011a;). ATP citrate lyase is required for normal sexual and asexual development in Gibberella zeae. Fungal Genet Biol48:408–417 [CrossRef][PubMed]
    [Google Scholar]
  42. Son H., Seo Y.-S., Min K., Park A. R., Lee J., Jin J.-M., Lin Y., Cao P., Hong S.-Y. et al. ( 2011b;). A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathog7:e1002310 [CrossRef][PubMed]
    [Google Scholar]
  43. Strauss J., Reyes-Dominguez Y.. ( 2011;). Regulation of secondary metabolism by chromatin structure and epigenetic codes. Fungal Genet Biol48:62–69 [CrossRef][PubMed]
    [Google Scholar]
  44. Tatusov R. L., Galperin M. Y., Natale D. A., Koonin E. V.. ( 2000;). The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res28:33–36 [CrossRef][PubMed]
    [Google Scholar]
  45. Turgeon B. G., Garber R. C., Yoder O. C.. ( 1987;). Development of a fungal transformation system based on selection of sequences with promoter activity. Mol Cell Biol7:3297–3305[PubMed]
    [Google Scholar]
  46. Wiemann P., Brown D. W., Kleigrewe K., Bok J. W., Keller N. P., Humpf H.-U., Tudzynski B.. ( 2010;). FfVel1 and FfLae1, components of a velvet-like complex in Fusarium fujikuroi, affect differentiation, secondary metabolism and virulence. Mol Microbiol77:972–994[PubMed]
    [Google Scholar]
  47. Yu J.-H., Hamari Z., Han K.-H., Seo J.-A., Reyes-Domínguez Y., Scazzocchio C.. ( 2004;). Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet Biol41:973–981 [CrossRef][PubMed]
    [Google Scholar]
  48. Yu H.-Y., Seo J.-A., Kim J.-E., Han K.-H., Shim W.-B., Yun S.-H., Lee Y.-W.. ( 2008;). Functional analyses of heterotrimeric G protein G α and G β subunits in Gibberella zeae. Microbiology154:392–401 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.059188-0
Loading
/content/journal/micro/10.1099/mic.0.059188-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error