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
2019-10-19
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.
  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 H. R. Hohl & G. Turian. New York: Academic Press.
  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 A. F. Rowley, H. Kuhn & T. Schewe. Princeton, NJ: Princeton University Press.
  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 M. A. Innis, D. H. Gelfand, J. S. Sninsky & T. J. White. San Diego, CA: Academic Press.
  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.
  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 S. A. Leong, C. Allen & E. W. Triplet. St Paul, MN: International Society for Plant –Microbe Interactions.
  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