1887

Abstract

Oxylipins called psi factors have been shown to alter the ratio of asexual to sexual sporulation in the filamentous fungus . Analysis of the genome has led to the identification of three fatty acid oxygenases (PpoA, PpoB and PpoC) predicted to produce psi factors. Here, it is reported that deletion of ) reduced production of the oleic-acid-derived oxylipin psiB and increased the ratio of asexual to sexual spore development. Generation of the triple mutant ΔΔΔ resulted in a strain deficient in producing oleic- and linoleic-acid-derived 8′-hydroxy psi factor and caused increased and mis-scheduled activation of sexual development. Changes in asexual to sexual spore development were positively correlated to alterations in the expression of and , respectively. PpoB and/or its products antagonistically mediate the expression levels of and , thus revealing regulatory feedback loops among these three genes. Phylogenetic analyses showed that genes are present in both saprophytic and pathogenic Ascomycetes and Basidiomycetes, suggesting a conserved role for Ppo enzymes in the life cycle of fungi.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27880-0
2005-06-01
2021-07-31
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/6/mic1511809.html?itemId=/content/journal/micro/10.1099/mic.0.27880-0&mimeType=html&fmt=ahah

References

  1. Abell B. M., Holbrook L. A., Abenes M., Murphy D. J., Hills M. J., Moloney M. M. 1997; Role of the proline knot motif in oleosin endoplasmic reticulum topology and oil body targeting. Plant Cell 9:1481–1493 [CrossRef]
    [Google Scholar]
  2. Adams T. H., Boylan M. T., Timberlake W. E. 1988; brlA is necessary and sufficient to direct conidiophore development in Aspergillus nidulans. Cell 54:353–362 [CrossRef]
    [Google Scholar]
  3. Adams T. H., Wieser J. K., Yu J. H. 1998; Asexual sporulation in Aspergillus nidulans. Microbiol Mol Biol Rev 62:35–54
    [Google Scholar]
  4. Agrios G. N. 1997 Plant Pathology, 4th edn. San Diego, CA: Academic Press;
    [Google Scholar]
  5. Alexopoulos C. J., Mims C. W., Blackwell M. 1996 Introductory Mycology , 4th edn. Chichester: Wiley;
  6. Blee E. 2002; Impact of phyto-oxylipins in plant defense. Trends Plant Sci 7:315–322 [CrossRef]
    [Google Scholar]
  7. Browse J., McCourt P. J., Somerville C. R. 1986; Fatty acid composition of leaf lipids determined after combined digestion and fatty acid methyl ester formation from fresh tissue. Anal Biochem 152:141–145 [CrossRef]
    [Google Scholar]
  8. Burow G. B., Gardner H. W., Keller N. P. 2000; A peanut seed lipoxygenase responsive to Aspergillus colonization. Plant Mol Biol 42:689–701 [CrossRef]
    [Google Scholar]
  9. Calvo A. M., Hinze L. L., Gardner H. W., Keller N. P. 1999; Sporogenic effect of polyunsaturated fatty acids on development of Aspergillus spp. Appl Environ Microbiol 65:3668–3673
    [Google Scholar]
  10. Calvo A. M., Gardner H. W., Keller N. P. 2001; Genetic connection between fatty acid metabolism and sporulation in Aspergillus nidulans. J Biol Chem 276:25766–25774 [CrossRef]
    [Google Scholar]
  11. Calvo A. M., Wilson R. A., Bok J. W., Keller N. P. 2002; Relationship between secondary metabolism and fungal development. Microbiol Mol Biol Rev 66:447–459 [CrossRef]
    [Google Scholar]
  12. Champe S. P., el-Zayat A. A. 1989; Isolation of a sexual sporulation hormone from Aspergillus nidulans. J Bacteriol 171:3982–3988
    [Google Scholar]
  13. Champe S. P., Kurtz M. B., Yager L. N., Butnick N. Z., Axelrod D. E. 1981; Spore formation in Aspergillus nidulans: competence and other developmental processes. In The Fungal Spores: Morphogenic Controls pp 255–276 Edited by Hohl H. R., Turian G. New York: Academic Press;
    [Google Scholar]
  14. Champe S. P., Rao P., Chang A. 1987; An endogenous inducer of sexual development in Aspergillus nidulans. J Gen Microbiol 133:1383–1387
    [Google Scholar]
  15. Champe S. P., Nagle D. L., Yager L. N. 1994; Sexual sporulation. Prog Ind Microbiol 29:429–454
    [Google Scholar]
  16. Chen J. C., Tzen J. T. 2001; An in vitro system to examine the effective phospholipids and structural domain for protein targeting to seed oil bodies. Plant Cell Physiol 42:1245–1252 [CrossRef]
    [Google Scholar]
  17. Chenna R., Sugawara H., Koike T., Lopez R., Gibson T. J., Higgins J. D. 2003; Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500 [CrossRef]
    [Google Scholar]
  18. Farmer E. E., Almeras E., Krishnamurthy V. 2003; Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6:372–378 [CrossRef]
    [Google Scholar]
  19. Fox S. R., Akpinar A., Prabhune A. A., Friend J., Ratledge C. 2000; The biosynthesis of oxylipins of linoleic and arachidonic acids by the sewage fungus Leptomitus lacteus, including the identification of 8R-hydroxy-9Z,12Z-octadecadienoic acid. Lipids 35:23–30 [CrossRef]
    [Google Scholar]
  20. Funk C. D. 2001; Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294:1871–1875 [CrossRef]
    [Google Scholar]
  21. Goodrich-Tanrikulu M., Howe K., Stafford A., Nelson M. A. 1998; Changes in fatty acid composition of Neurospora crassa accompany sexual development and ascospore germination. Microbiology 144:1713–1720 [CrossRef]
    [Google Scholar]
  22. Han K.-H., Han K. Y., Yu J. H., Chae K. S., Jahng K. Y., Han D. M. 2001; The nsdD gene encodes a putative GATA-type transcription factor necessary for sexual development of Aspergillus nidulans. Mol Microbiol 41:299–309 [CrossRef]
    [Google Scholar]
  23. Herman R. P. 1998; Oxylipin production and action in fungi and related organisms. In Eicosanoids and Related Compounds in Plants and Animals pp 115–130 Edited by Rowley A. F., Kuhn H., Schewe T. Princeton, NJ: Princeton University Press;
    [Google Scholar]
  24. Hornsten L., Su C., Osbourn A. E., Garosi P., Hellman U., Wernstedt C., Oliw E. H. 1999; Cloning of linoleate diol synthase reveals homology with prostaglandin H synthases. J Biol Chem 274:28219–28224 [CrossRef]
    [Google Scholar]
  25. Howe G. A., Schilmiller A. L. 2002; Oxylipin metabolism in response to stress. Curr Opin Plant Biol 5:230–236 [CrossRef]
    [Google Scholar]
  26. Huber S. M., Lottspeich F., Kamper J. 2002; A gene that encodes a product with similarity to dioxygenases is highly expressed in teliospores of Ustilago maydis. Mol Genet Genomics 267:757–771 [CrossRef]
    [Google Scholar]
  27. Jensen E. C., Ogg C., Nickerson K. W. 1992; Lipoxygenase inhibitors shift the yeast/mycelium dimorphism in Ceratocystis ulmi . Appl Environ Microbiol 58:2505–2508
    [Google Scholar]
  28. Kerwin J. L., Simmons C. A., Washino R. K. 1986; Eicosanoid regulation of oosporogenesis by Lagenidium giganteum . Prostaglandins Leukot Med 23:173–178 [CrossRef]
    [Google Scholar]
  29. Kim H., Han K., Kim K., Han D., Jahng K., Chae K. 2002; The veA gene activates sexual development in Aspergillus nidulans. Fungal Genet Biol 37:72–80 [CrossRef]
    [Google Scholar]
  30. Kock J. L., Venter P., Linke D., Schewe T., Nigam S. 1998; Biological dynamics and distribution of 3-hydroxy fatty acids in the yeast Dipodascopsis uninucleata as investigated by immunofluorescence microscopy. Evidence for a putative regulatory role in the sexual reproductive cycle. FEBS Lett 427:345–348 [CrossRef]
    [Google Scholar]
  31. Kock J. L., Strauss C. J., Pohl C. H., Nigam S. 2003; The distribution of 3-hydroxy oxylipins in fungi. Prostaglandins Other Lipid Mediat 71:85–96 [CrossRef]
    [Google Scholar]
  32. Lee B. S., Taylor J. W. 1990; Isolation of DNA from fungal mycelia and single spores. In PCR Protocols: a Guide to Methods and Applications pp 282–287 Edited by Innis M. A., Gelfand D. H., Sninsky J. S., White T. J. San Diego, CA: Academic Press;
    [Google Scholar]
  33. Mazur P., Meyers H. V., Nakanishi K. 1990; Structural elucidation of sporogenic fatty acid metabolites from Aspergillus nidulans. Tetrahedron Lett 31:3837–3840 [CrossRef]
    [Google Scholar]
  34. Mazur P., Nakanishi K., El-Zayat A. A. E., Champe S. P. 1991; Structure and synthesis of sporogenic psi factors from Aspergillus nidulans. J Chem Soc Chem Commun 20:1486–1487
    [Google Scholar]
  35. Noverr M. C., Erb-Downward J. R., Huffnagle G. B. 2003; Production of eicosanoids and other oxylipins by pathogenic eukaryotic microbes. Clin Microbiol Rev 16:517–533 [CrossRef]
    [Google Scholar]
  36. Nukima M. T., Sassa M., Ikeda M., Takahashi K. 1981; Linoleic acid enhances perithecial production in Neurospora crassa . Agric Biol Chem 45:2371–2373 [CrossRef]
    [Google Scholar]
  37. Osmani A. H., May G. S., Osmani S. A. 1999; The extremely conserved pyroA gene of Aspergillus nidulans is required for pyridoxine synthesis and is required indirectly for resistance to photosensitizers. J Biol Chem 274:23565–23569 [CrossRef]
    [Google Scholar]
  38. Pontecorvo G., Roper J. A., Hemmons L. M., MacDonald K. D., Bufton A. W. J. 1953; The genetics of Aspergillus nidulans. Adv Genet 5:141–239
    [Google Scholar]
  39. Prade R. A., Timberlake W. E. 1993; The Aspergillus nidulans brlA regulatory locus consists of overlapping transcription units that are individually required for conidiophore development. EMBO J 12:2439–2447
    [Google Scholar]
  40. Roeder P. E., Sargent M. L., Brody S. 1982; Circadian rhythms in Neurospora crassa: oscillations in fatty acids. Biochemistry 21:4909–4916 [CrossRef]
    [Google Scholar]
  41. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  42. Strauss T., Botha A., Kock J. L., Paul I., Smith D. P., Linke D., Schewe T., Nigam S. 2000; Mapping the distribution of 3-hydroxylipins in the Mucorales using immunofluorescence microscopy. Antonie Van Leeuwenhoek 78:39–42 [CrossRef]
    [Google Scholar]
  43. Su C., Oliw E. H. 1996; Purification and characterization of linoleate 8-dioxygenase from the fungus Gaeumannomyces graminis as a novel hemoprotein. J Biol Chem 271:14112–14118 [CrossRef]
    [Google Scholar]
  44. Tsitsigiannis D. I., Wilson R. A., Keller N. P. 2002; Lipid mediated signaling in the Aspergillus/seed interaction. In Biology of Plant–Microbe Interactions pp 186–191 Edited by Leong S. A., Allen C., Triplet E. W. St Paul, MN: International Society for Plant –Microbe Interactions;
    [Google Scholar]
  45. Tsitsigiannis D. I., Kowieski T. M., Zarnowski R., Keller N. P. 2004a; Lipogenic signals act as developmental regulators of spore balance in Aspergillus nidulans. Eukaryot Cell 3:1398–1411 [CrossRef]
    [Google Scholar]
  46. Tsitsigiannis D. I., Zarnowski R., Keller N. P. 2004b; The lipid body protein, PpoA, coordinates sexual and asexual sporulation in Aspergillus nidulans. J Biol Chem 279:11344–11353 [CrossRef]
    [Google Scholar]
  47. Wieser J., Adams T. H. 1995; flbD encodes a Myb-like DNA-binding protein that coordinates initiation of Aspergillus nidulans conidiophore development. Genes Dev 9:491–502 [CrossRef]
    [Google Scholar]
  48. Wilson R. A., Calvo A. M., Chang P.-K., Keller N. P. 2004; Characterization of the Aspergillus parasiticus Δ12-desaturase gene: a role for lipid metabolism in the Aspergillus/seed interaction. Microbiology 150:2881–2888 [CrossRef]
    [Google Scholar]
  49. Yelton M. M., Hamer J. E., Timberlake W. E. 1984; Transformation of Aspergillus nidulans by using a trpC plasmid. Proc Natl Acad Sci U S A 81:1470–1474 [CrossRef]
    [Google Scholar]
  50. Zarnowski R., Suzuki Y., Esumi Y., Pietr S. J. 2000; 5-n-Alkylresorcinols from the green microalga. Apatococcus constipatus Phytochemistry 55:975–977 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27880-0
Loading
/content/journal/micro/10.1099/mic.0.27880-0
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