1887

Abstract

SUMMARY: A tip-high Ca2+ gradient is observed in growing fungal hyphae, but so far its role remains unknown. A mathematical model is presented, which provides evidence for the functions of such a Ca2+ gradient, in terms of its non-linear effect on the visco-elastic properties of the hyphal cytoskeleton. The model explains how the Ca2+ status at the tip may be responsible for the apical accumulation of vesicles and for an increase in the cytogel osmotic pressure, accompanied by the contraction of the cytoskeleton. The experimentally observed retraction of the spitzenkarper preceding the initiation of a branch is also reproduced, by simulating a subapical transient release of Cat+ from internal stores.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-144-10-2771
1998-10-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/144/10/mic-144-10-2771.html?itemId=/content/journal/micro/10.1099/00221287-144-10-2771&mimeType=html&fmt=ahah

References

  1. Bartnicki-Garcia S., Bartnicki D., Gierz G., López-Franco R., Bracker C. 1995a; Evidence that the Spitzenkörper behavior determines the shape of a fungal hypha: a test of the hyphoid model.. Exp Mycol 19:153–159
    [Google Scholar]
  2. Bartnicki-Garcia S., Gierz G., Bartnicki D., López-Franco R., Bracker C. 1995b; Disruption of tip growth in hyphae of Rhizoctonia solani: an experimental test of the hyphoid model.. In Proceedings of the Annual Meeting of the Mycological Society of America 1995
    [Google Scholar]
  3. Cornelius G., Nakashima H. 1987; Vacuoles play a decisive role in calcium homeostasis in Neurospora crassa.. J Gen Microbiol 133:2341–2347
    [Google Scholar]
  4. Deloubresse N., Klotz C., Vigues B., Rutin J., Beisson J. 1991; Ca2+-binding proteins and contractility of the infracillary latice in Paramecium.. Biol Cell 71:217–225
    [Google Scholar]
  5. Dicker J., Turian G. 1990; Calcium deficiencies and apical hyperbranching in wild type and the ̒frost̓ and ̒spray̓ morphological mutants of Neurospora crassa.. J Gen Microbiol 136:1413–1420
    [Google Scholar]
  6. Garrill A., Jackson S., Lew R., Heath I. 1993; Ion channel activity and tip growth: tip-localized stretch-activated channels generate an essential Ca2+ gradient in the oomycete Saprolegnia ferax.. Eur J Cell Biol 60:358–365
    [Google Scholar]
  7. Gollnick F., Meyer R., Stockem W. 1991; Visualization and measurement of calcium transients in Amoeba proteus by fura-2 fluorescence.. Eur J Cell Biol 55:262–271
    [Google Scholar]
  8. Goodwin B., Trainor L. 1985; Tip and whorl morphogenesis in Acetabularia by calcium regulated strain fields.. J Theor Biol 117:79–106
    [Google Scholar]
  9. Gow N. 1995; Tip growth and polarity.. In The Growing Fungus pp. 277–299 Gow N., Gadd G. Edited by London:: Chapman & Hall.;
    [Google Scholar]
  10. Gow N., Miller P., Gooday G. 1992; Life at the apex: growth of the hyphal tip.. J Chem Tecbnol Biotechnol 56:217–219
    [Google Scholar]
  11. Grove S., Sweigard J. 1981; The Spitzenkörper core persists after tip growth is arrested by cytochalasins.. Mycol Soc Am Newsl 32:33
    [Google Scholar]
  12. Harold F. 1994; Ionic and electrical dimensions of hyphal growth.. In The Mycota. Growth, Differentiation and Sexuality 1 pp. 89–109 Wessels J.G.H., Meinhardt F. Edited by Berlin & Heidelberg:: Springer.;
    [Google Scholar]
  13. Harold R., Harold F. 1986; Ionophores and cytochalasins modulate branching in Achyla bisexualis.. J Gen Microbiol 132:213–219
    [Google Scholar]
  14. Heath I. 1995; The cytoskeleton.. In The Growing Fungus pp. 99–134 Gow N., Gadd G. Edited by London:: Chapman & Hall.;
    [Google Scholar]
  15. Hyde G., Heath I. 1997; Ca2+ gradients in hyphae and branches of Saprolegnia ferax.. Fungal Genet Biol 21:238–251
    [Google Scholar]
  16. Jackson S., Heath I. 1989; Effects of exogenous calcium ions on tip growth, intracellular Ca2+ concentration, and actin arrays in hyphae of the fungus Saprolegnia ferax.. Exp Mycol 13:1–12
    [Google Scholar]
  17. Jackson S., Heath I. 1992; UV microirradiation elicits Ca2+-dependent apex-directed cytoplasmic contractions in hyphae.. Protoplasma 170:46–52
    [Google Scholar]
  18. Jackson S., Heath I. 1993; Roles of calcium ions in hyphal tip growth.. Microbiol Rev 57:367–382
    [Google Scholar]
  19. Janmey P. 5 other authors 1988; Viscoelasticity of F actin and F-actin/gelsolin complexes.. Biochemistry 27:8218–8226
    [Google Scholar]
  20. Janmey P., Euteneur U., Traub P., Schllwa M. 1991; Viscoelastic properties of vimentin compared with other filamentous biopolymer networks.. J Cell Biol 113:155–160
    [Google Scholar]
  21. Kaminskyj S., Jackson S., Heath I. 1992; Fixation induces differential polarized translocations of organelles in hyphae of Saprolegnia ferax.. J Microsc 167:153–168
    [Google Scholar]
  22. Levina N., Lew R., Hyde G., Heath I. 1995; The roles of Ca2+and plasmamembrane ion channels in hyphal tip growth of Neurospora crassa.. J Cell Sci 108:3405–3417
    [Google Scholar]
  23. Lopez-Franco R., Bracker C. 1996; Diversity and dynamics of the Spitzenkörper in growing hyphal tips of higher fungi.. Protoplasma 195:90–111
    [Google Scholar]
  24. Luby-Phelps K. 1994; Physical properties of cytoplasm.. Curr Opin Cell Biol 6:3–9
    [Google Scholar]
  25. McGoldrick C., Gruver C., May G. 1995; myoA of Aspergillus nidulans encodes an essential myosin I required for secretion and polarized growth.. J Cell Biol 128:577–587
    [Google Scholar]
  26. McKerracher L., Heath I. 1986a; Fungal nuclear behavior analysed by ultraviolet microbeam irradiation.. Cell Motil Cytoskeleton 6:35–47
    [Google Scholar]
  27. McKerracher L., Heath I. 1986b; Polarized cytoplasmic movement and inhibition of saltations induced by calciummediated effects of microbeams in fungal hyphae.. Cell Motil Cytoskeleton 6:136–145
    [Google Scholar]
  28. McKerracher L., Heath I. 1987; Cytoplasmic migration and intracellular organelle movements during tip growth of fungal hyphae.. Exp Mycol 11:79–100
    [Google Scholar]
  29. Miller A., Vogg G., Saunders D. 1990; Cytosolic calcium homeostasis in fungi: roles of plasma membrane transport and intracellular sequestration of calcium.. Proc Natl Acad Sci USA 87:9348–9352
    [Google Scholar]
  30. Murphy D., Bracker C. 1996; Effects of electric fields on hyphal growth and Spitzenkörper in Rhtioctonia solani. . In Proceedings of the Annual Meeting of the Mycological Society of America 1996
    [Google Scholar]
  31. Odell G. 1977; A continuum theory of Allen̓s frontal con-traction model of amoeboid pseudopodium extension.. J Mechanochem Cell Motil 4:1–13
    [Google Scholar]
  32. Oster G. 1984; On the crawling of cells.. J Embryol Exp Morphol Suppl 83:329–364
    [Google Scholar]
  33. Oster G., Murray J., Harris A. 1983; Mechanical aspects of mesenchymal morphogenesis.. J Embryol Exp Morphol 78:83–125
    [Google Scholar]
  34. Pollard T., Cooper J. 1986; Actin and actin-binding proteins. A critical evaluation of mechanism and functions.. Annu Rev Biochem 55:987–1035
    [Google Scholar]
  35. Read N., Allan W., Knight H., Knight M., Malho R., Russell A., Shacklock P., Trewavas A. 1992a; Imaging and measurement of cytosolic free calcium in plant and fungal cells.. J Microsc 166:57–86
    [Google Scholar]
  36. Read N., Knight H., Trewavas A. 1992b; Fluorescence ratio imaging and confocal microscopy of calcium in filamentous fungi.. Binary 4:50–52
    [Google Scholar]
  37. Regalado C. 1997 Mechanistic models for colony form in filamentous fungi. PhD thesis University of Dundee.:
    [Google Scholar]
  38. Regalado C., Sleeman B., Ritz K. 1997; Aggregation and collapse of fungal wall vesicles in hyphal tips: a model for the origin of the Spitzenkörper.. Philos Trans R Soc Lond B 352:1963–1974
    [Google Scholar]
  39. Reissig J., Kinney S. 1983; Calcium as a branching signal in Neurospora crassa.. J Bacteriol 154:1397–1402
    [Google Scholar]
  40. Reynaga-Peña C., Bracker C., Bartnicki-Garcia S. 1995; Cytoplasmic contractions, spitzenkörper behavior and apicalbranching in Aspergillus niger.. In Proceedings of the Annual Meeting of the Mycological Society of America 1995
    [Google Scholar]
  41. Reynaga-Peña C, López-Franco R., Bracker C., Bartnicki-Garcia S. 1996; Cytoplasmic contractions in fungal hyphae and their morphogenetic consequences.. In Proceedings of the Annual Meeting of the Mycological Society of America 1996
    [Google Scholar]
  42. Reynaga-Peña C., Gierz G., Bartnicki-Garcia S. 1997; Analysis of the role of the spitzenkörper in fungal morphogenesis by computer simulation of apical branching in Aspergillus niger.. Proc Natl Acad Sci USA 94:9096–9101
    [Google Scholar]
  43. Robson G., Wiebe M., Trinci A. 1991; Low calcium concentrations induce increased branching in Fusarium graminearum.. Mycol Res 95:561–565
    [Google Scholar]
  44. Schmid J., Harold F. 1988; Dual role for calcium ions in apical growth of Neurospora crassa.. J Gen Microbiol 134:2623–2631
    [Google Scholar]
  45. Tagawa T., Bonner J. 1957; Mechanical properties of the Avena coleoptile as related to auxin and to ionic interactions.. Plant Physiol 32:207–212
    [Google Scholar]
  46. Taylor D., Hellewell S., Virgin H., Heiple J. 1979; The solation-contraction coupling hypothesis of cell movements.. In Cell Motility: Molecules and Organization pp. 363–377 Hatano S. Edited by New York:: Academic Press.;
    [Google Scholar]
  47. Yin H., Zaner K., Stossel T. 1980; Ca2+ control of actin gelation. Interaction of gelsolin with actin filaments and regulation of actin gelation.. J Biol Chem 255:9494–9500
    [Google Scholar]
  48. Yuan S., Heath I. 1991; Chlortetracycline staining patterns of growing hyphal tips of the oomycete Saprolegnia ferax.. Exp Mycol 15:103–115
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-144-10-2771
Loading
/content/journal/micro/10.1099/00221287-144-10-2771
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