1887

Abstract

In the accompanying paper [ Cho, E.-M., Liu, L., Farmerie, W. & Keyhani, N. O. (2006) . 152, 2843–2854], the analysis of expressed sequence tag (EST) libraries derived from homogeneous single-cell populations of aerial conidia, blastospores and submerged conidia of the entomopathogenic fungus () has been reported. Here an extended EST analysis is presented of complex cell mixtures derived from fungal cells sporulating on chitin or grown under culture conditions inducing the production of the secondary metabolite, oosporein. Fungal material used for the construction of the libraries included germinating conidia and blastospores, mycelia, as well as cells in various developmental stages. Approximately 2500 5′ end sequences were determined from random sequencing of clones from each library, and were clustered into 277 contigs with 1069 singlets, and 306 contigs with 1064 singlets, for the chitin and oosporein libraries, respectively. Almost half (45–50 %) of the sequences in each library displayed either no significant similarity ( value >10) or similarity to hypothetical proteins found in the NCBI database. Approximately 20–25 % of the sequences in each library could be annotated by gene ontology terms. A comparative analysis between the two libraries, as well as the libraries in the accompanying paper, is presented. A set of 4360 clustered and unique sequences was characterized. The data are indicative of a highly plastic gene expression repertoire being available to for growth during different environmental and developmental conditions, and provides a dataset for gene discovery and genome annotation.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28845-0
2006-09-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/9/2855.html?itemId=/content/journal/micro/10.1099/mic.0.28845-0&mimeType=html&fmt=ahah

References

  1. Bagga S, Hu G, Screen S. E, St Leger R. J. 2004; Reconstructing the diversification of subtilisins in the pathogenic fungus Metarhizium anisopliae . Gene 324:159–169 [CrossRef]
    [Google Scholar]
  2. Basrai M. A, Lubkowitz M. A, Perry J. R, Miller D, Krainer E, Naider F, Becker J. M. 1995; Cloning of a Candida albicans peptide transport gene. Microbiology 141:1147–1156 [CrossRef]
    [Google Scholar]
  3. Bing L. A, Lewis L. C. 1992; Endophytic Beauveria bassiana (Balsamo) Vuillemin in corn: the influence of the plant growth stage and Ostrinia nubilalis (Hubner). Biocontrol Sci Technol 2:39–47 [CrossRef]
    [Google Scholar]
  4. Broome J. R, Sikorowski P. P, Norment B. R. 1976; A mechanism of pathogenicity of Beauveria bassiana on larvae of the imported fire ant, Solenopsis richteri . J Invertebr Pathol 28:87–91 [CrossRef]
    [Google Scholar]
  5. Brown G. D, Gordon S. 2005; Immune recognition of fungal β -glucans. Cell Microbiol 7:471–479 [CrossRef]
    [Google Scholar]
  6. Brownbridge M, Costa S, Jaronski S. T. 2001; Effects of in vitro passage of Beauveria bassiana on virulence to Bemisia argentifolii . J Invertebr Pathol 77:280–283 [CrossRef]
    [Google Scholar]
  7. Chang Y. D, Dickson R. C. 1988; Primary structure of the lactose permease gene from the yeast Kluyveromyces lactis . Presence of an unusual transcript structure. J Biol Chem 263:16696–16703
    [Google Scholar]
  8. Cho E.-M, Liu L, Farmerie W, Keyhani N. O. 2006; EST analysis of cDNA libraries from the entomopathogenic fungus Beauveria (Cordyceps) bassiana . I. Evidence for stage-specific gene expression in aerial conidia, in vitro blastospores and submerged conidia. Microbiology 152:2843–2854 [CrossRef]
    [Google Scholar]
  9. Clark T. B, Kellen W. R, Fukuda T, Lindegren J. E. 1968; Field and laboratory studies on the pathogenicity of the fungus Beauveria bassiana to three genera of mosquitoes. J Invertebr Pathol 11:1–7 [CrossRef]
    [Google Scholar]
  10. Clarkson J. M, Charnley A. K. 1996; New insights into the mechanisms of fungal pathogenesis in insects. Trends Microbiol 4:197–203 [CrossRef]
    [Google Scholar]
  11. Culliney T. W, Grace J. K. 2000; Prospects for the biological control of subterranean termites (Isoptera : rhinotermitidae), with special reference to Coptotermes formosanus . Bull Entomol Res 90:9–21 [CrossRef]
    [Google Scholar]
  12. De la Rosa W, Alatorre R, Barrera J. F, Toreillo C. 2000; Effect of Beauveria bassiana and Metarhizium anisopliae (Deuteromycetes) upon the coffee berry borer (Coleoptera : Scolytidae) under field conditions. J Econ Entomol 93:1409–1414 [CrossRef]
    [Google Scholar]
  13. El Basyouni S. H, Vining L. C. 1966; Biosynthesis of oosporein in Beauveria bassiana (Bals.) Vuill. Can J Biochem 44:557–565 [CrossRef]
    [Google Scholar]
  14. Farmerie W, Hammer J, Liu L, Sahni A, Scneider M. 2005; Biological workflow with BlastQuest. Data Knowledge Engineer 53:75–97 [CrossRef]
    [Google Scholar]
  15. Ferron P. 1981; Pest control by the fungi Beauveria and Metarhizium. In Microbial Control of Pests and Plant Diseases 1970–1980 pp  465–482 Edited by Burges H. D. New York: Academic Press;
    [Google Scholar]
  16. Freimoser F. M, Screen S, Bagga S, Hu G, St Leger R. J. 2003a; Expressed sequence tag (EST) analysis of two subspecies of Metarhizium anisopliae reveals a plethora of secreted proteins with potential activity in insect hosts. Microbiology 149:239–247 [CrossRef]
    [Google Scholar]
  17. Freimoser F. M, Screen S, Hu G, St Leger R. 2003b; EST analysis of genes expressed by the zygomycete pathogen Conidiobolus coronatus during growth on insect cuticle. Microbiology 149:1893–1900 [CrossRef]
    [Google Scholar]
  18. Freimoser F. M, Hu G, St Leger R. J. 2005; Variation in gene expression patterns as the insect pathogen Metarhizium anisopliae adapts to different host cuticles or nutrient deprivation in vitro . Microbiology 151:361–371 [CrossRef]
    [Google Scholar]
  19. Fujimura-Kamada K, Nouvet F. J, Michaelis S. 1997; A novel membrane-associated metalloprotease, Ste24p, is required for the first step of NH[sub]2[/sub]-terminal processing of the yeast a-factor precursor. J Cell Biol 136:271–285 [CrossRef]
    [Google Scholar]
  20. Gillespie J. P, Bailey A. M, Cobb B, Vilcinskas A. 2000; Fungi as elicitors of insect immune responses. Arch Insect Biochem Physiol 44:49–68 [CrossRef]
    [Google Scholar]
  21. Glinski M, Urbanke C, Hornbogen T, Zocher R. 2002; Enniatin synthetase is a monomer with extended structure: evidence for an intramolecular reaction mechanism. Arch Microbiol 178:267–273 [CrossRef]
    [Google Scholar]
  22. Grogan G. J, Holland H. L. 2000; The biocatalytic reactions of Beauveria spp. J Mol Catal B Enzym 9:1–32 [CrossRef]
    [Google Scholar]
  23. Gum J. R. Jr, Hicks J. W, Toribara N. W, Siddiki B, Kim Y. S. 1994; Molecular cloning of human intestinal mucin (MUC2) cDNA. Identification of the amino terminus and overall sequence similarity to prepro-von Willebrand factor. J Biol Chem 269:2440–2446
    [Google Scholar]
  24. Gupta S. C, Leathers T. D, El-Sayed G. N, Ignoffo C. M. 1992; Insect cuticle-degrading enzymes from the entomogenous fungus Beauveria bassiana . Exp Mycol 16:132–137 [CrossRef]
    [Google Scholar]
  25. Haese A, Schubert M, Herrmann M, Zocher R. 1993; Molecular characterization of the enniatin synthetase gene encoding a multifunctional enzyme catalysing N -methyldepsipeptide formation in Fusarium scirpi . Mol Microbiol 7:905–914 [CrossRef]
    [Google Scholar]
  26. Han E. K, Cotty F, Sottas C, Jiang H, Michels C. A. 1995; Characterization of AGT1 encoding a general α -glucoside transporter from Saccharomyces . Mol Microbiol 17:1093–1107 [CrossRef]
    [Google Scholar]
  27. Harris M. A, Clark J, Ireland A. 56 other authors 2004; The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32:D258–D261 [CrossRef]
    [Google Scholar]
  28. Herrmann M, Zocher R, Haese A. 1996; Effect of disruption of the enniatin synthetase gene on the virulence of Fusarium avenaceum . Mol Plant Microbe Interact 9:226–232 [CrossRef]
    [Google Scholar]
  29. Inoue H, Kimura T, Makabe O, Takahashi K. 1991; The gene and deduced protein sequences of the zymogen of Aspergillus niger acid proteinase A. J Biol Chem 266:19484–19489
    [Google Scholar]
  30. Isaka M, Kittakoop P, Kirtikara K, Hywel-Jones N. L, Thebtaranonth Y. 2005; Bioactive substances from insect pathogenic fungi. Acc Chem Res 38:813–823 [CrossRef]
    [Google Scholar]
  31. Jeffs L. B, Khachatourians G. G. 1997; Toxic properties of Beauveria pigments on erythrocyte membranes. Toxicon 35:1351–1356 [CrossRef]
    [Google Scholar]
  32. Kagamizono T, Nishino E. Matsumoto & 8 other authors 1995; Bassiatin, a new platelet aggregation inhibitor produced by Beauveria bassiana K-717. J Antibiot 48:1407–1412 [CrossRef]
    [Google Scholar]
  33. Kamyar M, Rawnduzi P, Studenik C. R, Kouri K, Lemmens-Gruber R. 2004; Investigation of the electrophysiological properties of enniatins. Arch Biochem Biophys 429:215–223 [CrossRef]
    [Google Scholar]
  34. Khachatourians G. G. 1992; Virulence of five Beauveria strains, Paecilomyces farnosus , and Verticillium lecanii against the migratory grasshopper, Melanoplus sanguinipes . J Invertebr Pathol 59:212–214 [CrossRef]
    [Google Scholar]
  35. Kirkland B. H, Westwood G. S, Keyhani N. O. 2004; Pathogenicity of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae to Ixodidae tick species Dermacentor variabilis , Rhipicephalus sanguineus , and Ixodes scapularis . J Med Entomol 41:705–711 [CrossRef]
    [Google Scholar]
  36. Kirkland B. H, Eisa A, Keyhani N. O. 2005; Oxalic acid as a fungal acaracidal virulence factor. J Med Entomol 42:346–351 [CrossRef]
    [Google Scholar]
  37. Kucera M, Samsinakova A. 1968; Toxins of the entomophagous fungus Beauveria bassiana . J Invertebr Pathol 12:316–320 [CrossRef]
    [Google Scholar]
  38. Lawen A. 1996; Biosynthesis and mechanism of action of cyclosporins. Prog Med Chem 33:53–97
    [Google Scholar]
  39. Leathers T. D, Gupta S. C. 1993; Susceptibility of the eastern tent caterpillar (Malacosma americanum) to the entomogenous fungus Beauveria bassiana . J Invertebr Pathol 61:217–219 [CrossRef]
    [Google Scholar]
  40. Leathers T. D, Gupta S. C, Alexander N. J. 1993; Mycopesticides: status, challenges, and potential. J Ind Microbiol 12:69–75 [CrossRef]
    [Google Scholar]
  41. Lewis L. C, Bruck D. J, Gunnarson R. D, Bidne K. G. 2001; Assessment of plant pathogenicity of endophytic Beauveria bassiana in Bt transgenic and non-transgenic corn. Crop Sci 41:1395–1400 [CrossRef]
    [Google Scholar]
  42. McCoy C. W. 1990; Entomogenous fungi as microbial pesticides. In New Directions in Biological Control pp  139–159 Edited by Baker R. R., Dunn P. E. New York: A. R. Liss;
    [Google Scholar]
  43. McCreath K. J, Specht C. A, Robbins P. W. 1995; Molecular cloning and characterization of chitinase genes from Candida albicans . Proc Natl Acad Sci U S A 92:2544–2548 [CrossRef]
    [Google Scholar]
  44. Oda N, Gotoh Y, Oyama H, Murao S, Oda K, Tsuru D. 1998; Nucleotide sequence of the gene encoding the precursor protein of pepstatin insensitive acid protease B, scytalidopepsin B, from Scytalidium lignicolum . Biosci Biotechnol Biochem 62:1637–1639 [CrossRef]
    [Google Scholar]
  45. Pegram R. A, Wyatt R. D, Smith T. L. 1982; Oosporein-toxicosis in the turkey poultry. Avian Dis 26:47–59 [CrossRef]
    [Google Scholar]
  46. Pendland J. C, Boucias D. G. 1998; Characterization of monoclonal antibodies against cell wall epitopes of the insect pathogenic fungus, Nomuraea rileyi : differential binding to fungal surfaces and cross-reactivity with host hemocytes and basement membrane components. Eur J Cell Biol 75:118–127 [CrossRef]
    [Google Scholar]
  47. Pendland J. C, Hung S. Y, Boucias D. G. 1993; Evasion of host defense by in vivo -produced protoplast-like cells of the insect mycopathogen Beauveria bassiana . J Bacteriol 175:5962–5969
    [Google Scholar]
  48. Pfeifer T. A, Khachatourians G. G. 1993; Electrophoretic karyotype of the entomopathogenic deuteromycete Beauveria bassiana . J Invertebr Pathol 61:231–235 [CrossRef]
    [Google Scholar]
  49. Regenberg B, During-Olsen L, Kielland-Brandt M. C, Holmberg S. 1999; Substrate specificity and gene expression of the amino-acid permeases in Saccharomyces cerevisiae . Curr Genet 36:317–328 [CrossRef]
    [Google Scholar]
  50. Roncero C. 2002; The genetic complexity of chitin synthesis in fungi. Curr Genet 41:367–378 [CrossRef]
    [Google Scholar]
  51. Ruiz-Herrera J, Gonzalez-Prieto J. M, Ruiz-Medrano R. 2002; Evolution and phylogenetic relationships of chitin synthases from yeasts and fungi. FEMS Yeast Res 1:247–256 [CrossRef]
    [Google Scholar]
  52. Seger C, Erlebach D, Stuppner H, Griesser U. J, Strasser H. 2005; Physicochemical properties of oosporein, the major secreted metabolite of the entomopathogenic fungus Beauveria brongniartii . Helv Chim Acta 88:802–810 [CrossRef]
    [Google Scholar]
  53. Sophianopoulou V, Scazzocchio C. 1989; The proline transport protein of Aspergillus nidulans is very similar to amino acid transporters of Saccharomyces cerevisiae . Mol Microbiol 3:705–714 [CrossRef]
    [Google Scholar]
  54. St Leger R, Charnley A. K, Cooper R. M. 1986; Cuticle-degrading enzymes from entomopathogenic fungi: synthesis in culture on cuticle. J Invertebr Pathol 48:85–95 [CrossRef]
    [Google Scholar]
  55. St Leger R, Joshi L, Bidochka M. J, Roberts D. W. 1996; Construction of an improved mycoinsecticide overexpressing a toxic protease. Proc Natl Acad Sci U S A 93:6349–6354 [CrossRef]
    [Google Scholar]
  56. Takahashi S, Uchida K, Kakinuma N, Hashimoto R, Yanagisawa T, Nakagawa A. 1998; The structures of pyridovericin and pyridomacrolidin, new metabolites from the entomopathogenic fungus, Beauveria bassiana . J Antibiot 51:1051–1054 [CrossRef]
    [Google Scholar]
  57. Vasseur V, Van Montagu M, Goldman G. H. 1995; Trichoderma harzianum genes induced during growth on Rhizoctonia solani cell walls. Microbiology 141:767–774 [CrossRef]
    [Google Scholar]
  58. Viaud M, Couteaudier Y, Levis C, Riba G. 1996; Genome organization in Beauveria bassiana : electrophoretic karyotype, gene mapping and telomeric fingerprints. Fungal Genet Biol 20:175–183 [CrossRef]
    [Google Scholar]
  59. Wang C, St Leger R. J. 2005; Developmental and transcriptional responses to host and nonhost cuticles by the specific locust pathogen Metarhizium anisopliae var. acridum . Eukaryot Cell 4:937–947 [CrossRef]
    [Google Scholar]
  60. Wang C, Hu G, St Leger R. J. 2005; Differential gene expression by Metarhizium anisopliae growing in root exudate and host (Manduca sexta) cuticle or hemolymph reveals mechanisms of physiological adaptation. Fungal Genet Biol 42:704–718 [CrossRef]
    [Google Scholar]
  61. Wraight S. P, Carruthers R. I, Bradley C. A, Jaronski S. T, Lacey L. A, Wood P, Galaini-Wraight S. 1998; Pathogenicity of the entomopathogenic fungi Paecilomyces spp. and Beauveria bassiana against the silverleaf whitefly, Bemisia argentifolii . J Invertebr Pathol 71:217–226 [CrossRef]
    [Google Scholar]
  62. Zimmermann C. R, Johnson S. M, Martens G. W, White A. G, Pappagianis D. 1996; Cloning and expression of the complement fixation antigen-chitinase of Coccidioides immitis . Infect Immun 64:4967–4975
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28845-0
Loading
/content/journal/micro/10.1099/mic.0.28845-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

PDF

Supplementary material 3

PDF

Supplementary material 4

PDF

Supplementary material 5

PDF

Supplementary material 6

PDF

Supplementary material 7

PDF
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