1887

Abstract

Nematode-trapping fungi enter the parasitic stage by developing specific morphological structures called traps. The global patterns of gene expression in traps and mycelium of the fungus were compared. The trap of this fungus is a unicellular spherical structure called the knob, which develops on the apex of a hyphal branch. RNA was isolated from knobs and mycelium and hybridized to a cDNA array containing probes of 2822 EST clones of . Despite the fact that the knobs and mycelium were grown in the same medium, there were substantial differences in the patterns of genes expressed in the two cell types. In total, 23·3 % (657 of 2822) of the putative genes were differentially expressed in knobs versus mycelium. Several of these genes displayed sequence similarities to genes known to be involved in regulating morphogenesis and cell polarity in fungi. Among them were several putative homologues for small GTPases, such as , and , and a rho GDP dissociation inhibitor (). Several homologues to genes involved in stress response, protein synthesis and protein degradation, transcription, and carbon metabolism were also differentially expressed. In the last category, a glycogen phosphorylase () gene homologue, one of the most upregulated genes in the knobs as compared to mycelium, was characterized. A number of the genes that were differentially expressed in trap cells are also known to be regulated during the development of infection structures in plant-pathogenic fungi. Among them, a () gene homologue (designated ), which is specifically expressed in appressoria of the rice blast fungus, was characterized.

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2005-03-01
2024-04-19
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References

  1. Ahren D., Troein C., Johansson T., Tunlid A. 2004; phorest: a web-based tool for comparative analyses of EST data. Mol Ecol Notes 4:311–314 [CrossRef]
    [Google Scholar]
  2. Ahrén D., Ursing B. M., Tunlid A. 1998; Phylogeny of nematode-trapping fungi based on 18S rDNA sequences. FEMS Microbiol Lett 158:179–184 [CrossRef]
    [Google Scholar]
  3. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410 [CrossRef]
    [Google Scholar]
  4. Ayscough K. R. 1998; In vivo functions of actin-binding proteins. Curr Opin Cell Biol 10:102–111 [CrossRef]
    [Google Scholar]
  5. Barron G. L. 1977 The Nematode-Destroying Fungi Guelph, Canada: Lancester Press;
    [Google Scholar]
  6. Benson D. A., Karsch-Mizrachi I., Lipman D. J., Ostell J., Wheeler D. L. 2004; GenBank: update. Nucleic Acids Res 32:23–26
    [Google Scholar]
  7. Bourne H. R., Sanders D. A., McCormick F. 1991; The GTPase superfamily: conserved structure and molecular mechanism. Nature 349:117–127 [CrossRef]
    [Google Scholar]
  8. Boyce K. J., Hynes M. J., Andrianopoulos A. 2003; Control of morphogenesis and actin localization by the Penicillium marneffei RAC homolog. J Cell Sci 116:1249–1260 [CrossRef]
    [Google Scholar]
  9. Brenner S. 1974; The genetics of Caenorhabditis elegans. Genetics 77:71–94
    [Google Scholar]
  10. Dijksterhuis J., Veenhuis M., Harder W., Nordbring-Hertz B. 1994; Nematophagous fungi: physiological aspects and structure-function relationships. Adv Microb Physiol 36:111–143
    [Google Scholar]
  11. Emmons S. W., Klass M. R., Hirsh D. 1979; Analysis of the constancy of DNA sequences during development and evolution of the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A 76:1333–1337 [CrossRef]
    [Google Scholar]
  12. Erdmann R., Blobel G. 1995; Giant peroxisomes in oleic acid-induced Saccharomyces cerevisiae lacking the peroxisomal membrane protein Pmp27p. J Cell Biol 128:509–523 [CrossRef]
    [Google Scholar]
  13. Ewing B., Hillier L., Wendl M. C., Green P. 1998; Base-calling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Res 8:175–185 [CrossRef]
    [Google Scholar]
  14. Finegold A. A., Johnson D. I., Farnsworth C. C., Gelb M. H., Judd S. R., Glomset J. A., Tamanoi F. 1991; Protein geranylgeranyltransferase of Saccharomyces cerevisiae is specific for Cys-Xaa-Xaa-Leu motif proteins and requires the CDC43 gene product but not the DPR1 gene product. Proc Natl Acad Sci U S A 88:4448–4452 [CrossRef]
    [Google Scholar]
  15. Fletterick R. J., Madsen N. B. 1980; The structures and related functions of phosphorylase a. Annu Rev Biochem 49:31–61 [CrossRef]
    [Google Scholar]
  16. Friman E. 1993; Isolation of trap cells from the nematode-trapping fungus Dactylaria candida. Exp Mycol 17:368–370 [CrossRef]
    [Google Scholar]
  17. Grell M. N., Mouritzen P., Giese H. 2003; A Blumeria graminis gene family encoding proteins with a C-terminal variable region with homologues in pathogenic fungi. Gene 311:181–192 [CrossRef]
    [Google Scholar]
  18. Huang X. 1992; A contig assembly program based on sensitive detection of fragment overlaps. Genomics 14:18–25 [CrossRef]
    [Google Scholar]
  19. Hwang P. K., Fletterick R. J. 1986; Convergent and divergent evolution of regulatory sites in eukaryotic phosphorylases. Nature 324:80–84 [CrossRef]
    [Google Scholar]
  20. Johansson T., Erlandsson R., Lundeberg J., Tunlid A, Le Quéré A., Ahrén D., Söderström B., Uhlén M. 2004; Transcriptional responses of Paxillus involutus and Betula pendula during formation of ectomycorrhizal root tissue. Mol Plant–Microbe Interact 17:202–215 [CrossRef]
    [Google Scholar]
  21. Justesen A., Somerville S., Christiansen S., Giese H. 1996; Isolation and characterization of two novel genes expressed in germinating conidia of the obligate biotroph Erysiphe graminis f.sp.hordei . Gene 170:131–135 [CrossRef]
    [Google Scholar]
  22. Kerr M. K., Churchill G. A. 2001; Experimental design for gene expression microarrays. Biostatistics 2:183–201 [CrossRef]
    [Google Scholar]
  23. Koch G., Tanaka K., Masuda T., Yamochi W., Nonaka H., Takai Y. 1997; Association of the Rho family small GTP-binding proteins with Rho GDP dissociation inhibitor (Rho GDI) in Saccharomyces cerevisiae . Oncogene 15:417–422 [CrossRef]
    [Google Scholar]
  24. Kumar S., Tamura K., Jakobsen I. B., Nei M. 2001; MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245 [CrossRef]
    [Google Scholar]
  25. Lappalainen P., Drubin D. G. 1997; Cofilin promotes rapid actin filament turnover in vivo. Nature 388:78–82 [CrossRef]
    [Google Scholar]
  26. Larsen M. 2000; Prospects for controlling animal parasitic nematodes by predacious microfungi. Parasitology 120:121–131
    [Google Scholar]
  27. Livak K. J., Schmittgen T. D. 2001; Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408 [CrossRef]
    [Google Scholar]
  28. McCafferty H. R., Talbot N. J. 1998; Identification of three ubiquitin genes of the rice blast fungus Magnaporthe grisea, one of which is highly expressed during initial stages of plant colonisation. Curr Genet 33:352–361 [CrossRef]
    [Google Scholar]
  29. Mewes H. W., Frishman D., Gruber C. 7 other authors 2000; MIPS: a database for genomes and protein sequences. Nucleic Acids Res 28:37–40 [CrossRef]
    [Google Scholar]
  30. Nakano K., Hwang P. K., Fletterick R. J. 1986; Complete cDNA sequence for rabbit muscle glycogen phosphorylase. FEBS Lett 204:283–287 [CrossRef]
    [Google Scholar]
  31. Nordbring-Hertz B., Jansson H.-B., Friman E. 5 other authors 1995 Nematophagous fungi Film No C 1851 Göttingen, Germany: Institut für den Wissenschaftlichen Film;
    [Google Scholar]
  32. Palm D., Goerl R., Burger K. J. 1985; Evolution of catalytic and regulatory sites in phosphorylases. Nature 313:500–502 [CrossRef]
    [Google Scholar]
  33. Pearson W. R. 1994; Using the fasta program to search protein and DNA sequence databases. Methods Mol Biol 24:307–331
    [Google Scholar]
  34. Pruyne D., Bretscher A. 2000a; Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J Cell Sci 113:365–375
    [Google Scholar]
  35. Pruyne D., Bretscher A. 2000b; Polarization of cell growth in yeast. II. The role of the cortical actin cytoskeleton. J Cell Sci 113:571–585
    [Google Scholar]
  36. Rauyaree P., Choi W., Fang E., Blackmon B., Dean R. A. 2004; Genes expressed during early stages of rice infection with the rice blast fungus Magnaporthe grisea. Mol Plant Pathol 2:347–354
    [Google Scholar]
  37. Rozen S., Skaletsky H. 2000; Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols pp 365–386 Edited by Krawetz S., Misener S. Totowa, NJ: Humana Press;
    [Google Scholar]
  38. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406
    [Google Scholar]
  39. Stiekema W. J., Heidekamp F., Dirkse W. G., van Beckum J., de Haan P., ten Bosch C., Louwerse J. D. 1988; Molecular cloning and analysis of four potato tuber mRNA. Plant Mol Biol 11:255–269 [CrossRef]
    [Google Scholar]
  40. Takano Y., Choi W., Mitchell T. K., Okuno T., Dean R. A. 2004; Large scale parallel analysis of gene expression during infection-related morphogenesis of Magnaporthe grisea. Mol Plant Pathol 4:337–346
    [Google Scholar]
  41. Thines E., Weber R. W., Talbot N. J. 2000; MAP kinase and protein kinase A-dependent mobilization of triacylglycerol and glycogen during appressorium turgor generation by Magnaporthe grisea . Plant Cell 12:1703–1718
    [Google Scholar]
  42. Thomas S. W., Glaring M. A., Rasmussen S. W., Kinane J. T., Oliver R. P. 2002; Transcript profiling in the barley mildew pathogen Blumeria graminis by serial analysis of gene expression (SAGE. Mol Plant–Microbe Interact 15:847–856 [CrossRef]
    [Google Scholar]
  43. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [CrossRef]
    [Google Scholar]
  44. Tucker S. L., Talbot N. J. 2001; Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu Rev Phytopathol 39:385–417 [CrossRef]
    [Google Scholar]
  45. Tunlid A., Johansson T., Nordbring-Hertz B. 1991; Surface polymers of the nematode-trapping fungus Arthrobotrys oligospora.. J Gen Microbiol 137:1231–1240 [CrossRef]
    [Google Scholar]
  46. Viaud M. C., Balhadere P. V., Talbot N. J. 2002; A Magnaporthe grisea cyclophilin acts as a virulence determinant during plant infection. Plant Cell 14:917–930 [CrossRef]
    [Google Scholar]
  47. Wolfinger R. D., Gibson G., Wolfinger E. D., Bennett L., Hamadeh H., Bushel P., Afshari C., Paules R. S. 2001; Assessing gene significance from cDNA microarray expression data via mixed models. J Comput Biol 8:625–637 [CrossRef]
    [Google Scholar]
  48. Wu T. D. 2001; Analysing gene expression data from DNA microarrays to identify candidate genes. J Pathol 195:53–65 [CrossRef]
    [Google Scholar]
  49. Xue C., Park G., Choi W., Zheng L., Dean R. A., Xu J. R. 2002; Two novel fungal virulence genes specifically expressed in appressoria of the rice blast fungus. Plant Cell 14:2107–2119 [CrossRef]
    [Google Scholar]
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