1887

Abstract

The ascomycete fungus is a devastating plant pathogen for major cereal crops. Ascospores are produced via sexual reproduction and forcibly discharged from mature perithecia, which function as the primary inocula. Perithecium development involves complex cellular processes and is under polygenic control. In this study, a novel gene, , was found to be required for ascus wall development in . deletion mutants produced normal-shaped perithecia and ascospores, yet ascospores were observed to precociously germinate inside the perithecium. Moreover, deletions resulted in abnormal ascus walls that collapsed prior to ascospore discharge. Based on localization of GEA1 to plasma membrane, GEA1 may be directly involved in ascus wall biogenesis. This is the first report to identify a unique gene required for ascus wall development in .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.064287-0
2013-06-01
2024-12-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/6/1077.html?itemId=/content/journal/micro/10.1099/mic.0.064287-0&mimeType=html&fmt=ahah

References

  1. Beckett A.( 1981). The ultrastructure of septal pores and associated structures in the ascogenous hyphae and asci of Sordaria humana. Protoplasma 107:127–147 [View Article]
    [Google Scholar]
  2. Beckett A., Crawford R. M.( 1973). The development and fine structure of the ascus apex and its role during spore discharge in Xylaria longipes. New Phytol 72:357–369 [View Article]
    [Google Scholar]
  3. Bowden R. L., Leslie J. F.( 1999). Sexual recombination in Gibberella zeae. Phytopathology 89:182–188 [View Article][PubMed]
    [Google Scholar]
  4. Cappellini R. A., Peterson J. L.( 1965). Macroconidium formation in submerged cultures by a non-sporulating strain of Gibberella zeae. Mycologia 57:962–966 [View Article]
    [Google Scholar]
  5. Cavinder B., Trail F.( 2012). Role of Fig1, a component of the low-affinity calcium uptake system, in growth and sexual development of filamentous fungi. Eukaryot Cell 11:978–988 [View Article][PubMed]
    [Google Scholar]
  6. Cavinder B., Hamam A., Lew R. R., Trail F.( 2011). Mid1, a mechanosensitive calcium ion channel, affects growth, development, and ascospore discharge in the filamentous fungus Gibberella zeae. Eukaryot Cell 10:832–841 [View Article][PubMed]
    [Google Scholar]
  7. Cuomo C. A., Güldener U., Xu J.-R., Trail F., Turgeon B. G., Di Pietro A., Walton J. D., Ma L.-J., Baker S. E.& other authors ( 2007). The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317:1400–1402 [View Article][PubMed]
    [Google Scholar]
  8. Desjardins A. E.( 2006). Fusarium Mycotoxins: Chemistry, Genetics, and Biology St Paul, MN: APS Press;
    [Google Scholar]
  9. Desjardins A. E., Brown D. W., Yun S. H., Proctor R. H., Lee T., Plattner R. D., Lu S. W., Turgeon B. G.( 2004). Deletion and complementation of the mating type (MAT) locus of the wheat head blight pathogen Gibberella zeae. Appl Environ Microbiol 70:2437–2444 [View Article][PubMed]
    [Google Scholar]
  10. Dignani M. C., Anaissie E.( 2004). Human fusariosis. Clin Microbiol Infect 10:Suppl 167–75 [View Article][PubMed]
    [Google Scholar]
  11. Dyer P. S., Ingram D. S., Johnstone K.( 1992). The control of sexual morphogenesis in the ascomycotina. Biol Rev Camb Philos Soc 67:421–458 [View Article]
    [Google Scholar]
  12. Emanuelsson O., Nielsen H., Brunak S., von Heijne G.( 2000). Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016 [View Article][PubMed]
    [Google Scholar]
  13. Fisher M. C., Henk D. A., Briggs C. J., Brownstein J. S., Madoff L. C., McCraw S. L., Gurr S. J.( 2012). Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194 [View Article][PubMed]
    [Google Scholar]
  14. Goswami R. S., Kistler H. C.( 2004). Heading for disaster: Fusarium graminearum on cereal crops. Mol Plant Pathol 5:515–525 [View Article][PubMed]
    [Google Scholar]
  15. Güldener U., Seong K.-Y., Boddu J., Cho S., Trail F., Xu J.-R., Adam G., Mewes H. W., Muehlbauer G. J., Kistler H. C.( 2006). Development of a Fusarium graminearum Affymetrix GeneChip for profiling fungal gene expression in vitro and in planta. Fungal Genet Biol 43:316–325 [View Article][PubMed]
    [Google Scholar]
  16. Hallen H. E., Trail F.( 2008). The L-type calcium ion channel cch1 affects ascospore discharge and mycelial growth in the filamentous fungus Gibberella zeae (anamorph Fusarium graminearum). Eukaryot Cell 7:415–424 [View Article][PubMed]
    [Google Scholar]
  17. Hallen H. E., Huebner M., Shiu S.-H., Güldener U., Trail F.( 2007). Gene expression shifts during perithecium development in Gibberella zeae (anamorph Fusarium graminearum), with particular emphasis on ion transport proteins. Fungal Genet Biol 44:1146–1156 [View Article][PubMed]
    [Google Scholar]
  18. 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 Microbiol 63:768–779 [View Article][PubMed]
    [Google Scholar]
  19. Harris S. D.( 2005). Morphogenesis in germinating Fusarium graminearum macroconidia. Mycologia 97:880–887 [View Article][PubMed]
    [Google Scholar]
  20. Horwitz B. A., Sharon A., Lu S. W., Ritter V., Sandrock T. M., Yoder O. C., Turgeon B. G.( 1999). A G protein alpha subunit from Cochliobolus heterostrophus involved in mating and appressorium formation. Fungal Genet Biol 26:19–32 [View Article][PubMed]
    [Google Scholar]
  21. 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 Interact 15:1119–1127 [View Article][PubMed]
    [Google Scholar]
  22. 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 Genet 43:87–95[PubMed]
    [Google Scholar]
  23. 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 Microbiol 72:1645–1652 [View Article][PubMed]
    [Google Scholar]
  24. 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 Genet 55:449–459 [View Article][PubMed]
    [Google Scholar]
  25. Kunze I., Hensel G., Adler K., Bernard J., Neubohn B., Nilsson C., Stoltenburg R., Kohlwein S. D., Kunze G.( 1999). The green fluorescent protein targets secretory proteins to the yeast vacuole. Biochim Biophys Acta 1410:287–298 [View Article][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 Microbiol 50:145–152 [View Article][PubMed]
    [Google Scholar]
  27. Lee J., Chang I.-Y., Kim H., Yun S.-H., Leslie J. F., Lee Y.-W.( 2009a). Genetic diversity and fitness of Fusarium graminearum populations from rice in Korea. Appl Environ Microbiol 75:3289–3295 [View Article][PubMed]
    [Google Scholar]
  28. Lee S.-H., Lee J., Lee S., Park E.-H., Kim K.-W., Kim M.-D., Yun S.-H., Lee Y.-W.( 2009b). GzSNF1 is required for normal sexual and asexual development in the ascomycete Gibberella zeae. Eukaryot Cell 8:116–127 [View Article][PubMed]
    [Google Scholar]
  29. 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 Commun 401:48–52 [View Article][PubMed]
    [Google Scholar]
  30. 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 Cell 10:1043–1052 [View Article][PubMed]
    [Google Scholar]
  31. Lee J., Myong K., Kim J.-E., Kim H.-K., Yun S.-H., Lee Y.-W.( 2012). FgVelB globally regulates sexual reproduction, mycotoxin production and pathogenicity in the cereal pathogen Fusarium graminearum. Microbiology 158:1723–1733 [View Article][PubMed]
    [Google Scholar]
  32. Leslie J. F., Summerell B. A.( 2006). The Fusarium Laboratory Manual Ames, IA: Blackwell Publishing; [View Article]
    [Google Scholar]
  33. Lin Y., Son H., Lee J., Min K., Choi G. J., Kim J.-C., Lee Y.-W.( 2011). A putative transcription factor MYT1 is required for female fertility in the ascomycete Gibberella zeae. PLoS ONE 6:e25586 [View Article][PubMed]
    [Google Scholar]
  34. Lysøe E., Pasquali M., Breakspear A., Kistler H. C.( 2011). The transcription factor FgStuAp influences spore development, pathogenicity, and secondary metabolism in Fusarium graminearum. Mol Plant Microbe Interact 24:54–67 [View Article][PubMed]
    [Google Scholar]
  35. Min K., Lee J., Kim J.-C., Kim S. G., Kim Y. H., Vogel S., Trail F., Lee Y.-W.( 2010). A novel gene, ROA, is required for normal morphogenesis and discharge of ascospores in Gibberella zeae. Eukaryot Cell 9:1495–1503 [View Article][PubMed]
    [Google Scholar]
  36. 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 Interact 14:580–584 [View Article][PubMed]
    [Google Scholar]
  37. Nguyen T. V, Schäfer W., Bormann J.( 2012). The stress-activated protein kinase FgOS-2 is a key regulator in the life cycle of the cereal pathogen Fusarium graminearum. Mol Plant Microbe Interact 25:1142–1156 [View Article][PubMed]
    [Google Scholar]
  38. Nielsen H., Engelbrecht J., Brunak S., von Heijne G.( 1997). Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6 [View Article][PubMed]
    [Google Scholar]
  39. Park A. R., Cho A.-R., Seo J.-A., Min K., Son H., Lee J., Choi G. J., Kim J.-C., Lee Y.-W.( 2012). Functional analyses of regulators of G protein signaling in Gibberella zeae. Fungal Genet Biol 49:511–520 [View Article][PubMed]
    [Google Scholar]
  40. Parry D. W., Jenkinson P., McLeod L.( 1995). Fusarium ear blight (scab) in small grain cereals – a review. Plant Pathol 44:207–238 [View Article]
    [Google Scholar]
  41. Pöggeler S., Nowrousian M., Kück U.( 2006). Fruiting-body development in ascomycetes. The Mycota J325–355 Kües U., Fischer R. Berlin & Heidelberg: [View Article]
    [Google Scholar]
  42. Raju N. B.( 1980). Meiosis and ascospore genesis in Neurospora. Eur J Cell Biol 23:208–223[PubMed]
    [Google Scholar]
  43. Raju N. B.( 1987). A Neurospora mutant with abnormal croziers, giant ascospores, and asci having multiple apical pores. Mycologia 79:696–706 [View Article]
    [Google Scholar]
  44. Raju N. B.( 1988). Nonlinear asci without apical pores in the peak mutant of Neurospora. Mycologia 80:825–831 [View Article]
    [Google Scholar]
  45. Raju N. B.( 1992). Genetic control of the sexual cycle in Neurospora. Mycol Res 96:241–262 [View Article]
    [Google Scholar]
  46. Raju N. B.( 2008). Meiosis and ascospore development in Cochliobolus heterostrophus. Fungal Genet Biol 45:554–564 [View Article][PubMed]
    [Google Scholar]
  47. Raju N. B., Newmeyer D.( 1977). Giant ascospores and abnormal croziers in a mutant of Neurospora crassa. Exp Mycol 1:152–165 [View Article]
    [Google Scholar]
  48. Read N. D., Beckett A.( 1996). Ascus and ascospore morphogenesis. Mycol Res 100:1281–1314 [View Article]
    [Google Scholar]
  49. Reynolds E. S.( 1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212 [View Article][PubMed]
    [Google Scholar]
  50. Sambrook J., Russell D. W.( 2001). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
    [Google Scholar]
  51. 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 Biol 48:408–417 [View Article][PubMed]
    [Google Scholar]
  52. Son H., Min K., Lee J., Raju N. B., Lee Y.-W.( 2011b). Meiotic silencing in the homothallic fungus Gibberella zeae. Fungal Biol 115:1290–1302 [View Article][PubMed]
    [Google Scholar]
  53. Son H., Seo Y.-S., Min K., Park A. R., Lee J., Jin J.-M., Lin Y., Cao P., Hong S.-Y.& other authors ( 2011c). A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathog 7:e1002310 [View Article][PubMed]
    [Google Scholar]
  54. Son H., Lee J., Lee Y.-W.( 2012a). Mannitol induces the conversion of conidia to chlamydospore-like structures that confer enhanced tolerance to heat, drought, and UV in Gibberella zeae. Microbiol Res 167:608–615 [View Article][PubMed]
    [Google Scholar]
  55. Son H., Min K., Lee J., Choi G. J., Kim J.-C., Lee Y.-W.( 2012b). Mitochondrial carnitine-dependent acetyl coenzyme A transport is required for normal sexual and asexual development of the ascomycete Gibberella zeae. Eukaryot Cell 11:1143–1153 [View Article][PubMed]
    [Google Scholar]
  56. Son H., Min K., Lee J., Choi G. J., Kim J.-C., Lee Y.-W.( 2012c). Differential roles of pyruvate decarboxylase in aerial and embedded mycelia of the ascomycete Gibberella zeae. FEMS Microbiol Lett 329:123–130 [View Article][PubMed]
    [Google Scholar]
  57. Spurr A. R.( 1969). A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43 [View Article][PubMed]
    [Google Scholar]
  58. Sutton J. C.( 1982). Epidemiology of wheat head blight and maize ear rot caused by Fusarium graminearum. Can J Plant Pathol 4:195–209 [View Article]
    [Google Scholar]
  59. Thompson-Coffe C., Zickler D.( 1992). Three microtubule-organizing centers are required for ascus growth and sporulation in the fungus Sordaria macrospora. Cell Motil Cytoskeleton 22:257–273 [View Article]
    [Google Scholar]
  60. Trail F., Common R.( 2000). Perithecial development by Gibberella zeae: a light microscopy study. Mycologia 92:130–138 [View Article]
    [Google Scholar]
  61. Trail F., Xu H., Loranger R., Gadoury D.( 2002). Physiological and environmental aspects of ascospore discharge in Gibberella zeae (anamorph Fusarium graminearum). Mycologia 94:181–189 [View Article][PubMed]
    [Google Scholar]
  62. Trail F., Gaffoor I., Vogel S.( 2005). Ejection mechanics and trajectory of the ascospores of Gibberella zeae (anamorph Fuarium graminearum). Fungal Genet Biol 42:528–533 [View Article][PubMed]
    [Google Scholar]
  63. Wang C., Zhang S., Hou R., Zhao Z., Zheng Q., Xu Q., Zheng D., Wang G., Liu H.& other authors ( 2011). Functional analysis of the kinome of the wheat scab fungus Fusarium graminearum. PLoS Pathog 7:e1002460 [View Article][PubMed]
    [Google Scholar]
  64. Wong P., Walter M., Lee W., Mannhaupt G., Münsterkötter M., Mewes H.-W., Adam G., Güldener U.( 2011). FGDB: revisiting the genome annotation of the plant pathogen Fusarium graminearum. Nucleic Acids Res 39:Database issueD637–D639 [View Article][PubMed]
    [Google Scholar]
  65. 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 Biol 41:973–981 [View Article][PubMed]
    [Google Scholar]
  66. 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. Microbiology 154:392–401 [View Article][PubMed]
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.064287-0
Loading
/content/journal/micro/10.1099/mic.0.064287-0
Loading

Data & Media loading...

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