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Volume 149, Issue 9

Calcium gradient dependence of hyphal growth Free

Abstract

A tip-high cytoplasmic calcium gradient has been identified as a requirement for hyphal growth in the fungus . The Ca gradient is less steep compared to wall vesicle, wall incorporation and vesicular Ca gradients, but this can be explained by Ca diffusion. Analysis of the relation between the rate of hyphal growth and the spatial distribution of tip-localized calcium indicates that hyphal growth rates depend upon the tip-localized calcium concentration. It is not the steepness of the calcium gradient, but tip-localized calcium and the difference in tip-localized calcium versus subapical calcium concentration which correlate closely with hyphal growth rate. A minimal concentration difference between the apex and subapical region of 30 nM is required for growth to occur. The calcium concentration dependence of growth may relate directly to biochemical functions of calcium in hyphal extension, such as vesicle fusion and enzyme activation during cellular expansion. Initiation of tip growth may rely upon random Ca motions causing localized regions of elevated calcium. Continued hyphal expansion may activate a stretch-activated phospholipase C which would increase tip-localized inositol 1,4,5-trisphosphate (IP). Hyphal expansion, induced by mild hypoosmotic treatment, does increase diacylglycerol, the other product of phospholipase C activity. This is consistent with evidence that IP-activated Ca channels generate and maintain the tip-high calcium gradient.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): BAPTA, 1,2-bis(ortho-aminophenoxy)ethane-N,N,N′,N′-tetrapotassium acetate , CTC, chlortetracycline , fluo-3, 2,7-dichloro-6-hydroxy-3-oxo-9-xanthenyl-4′-methyl-2,2′-(ethylenedioxy)dianiline-N,N,N′,N′-tetraacetic acid and IP3, inositol 1,4,5-trisphosphate
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2003-09-01
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References

  1. Al-Baldawi N. F., Abercrombie R. F. 1995; Calcium diffusion coefficient in Myxicola axoplasm. Cell Calcium 17:430–438
     [Google Scholar]
  2. Bligh E. G., Dyer W. J. 1959; A rapid method of lipid extraction and purification. Can J Biochem Physiol 37:911–917
     [Google Scholar]
  3. Bocckino S. B., Blackmore P. F., Exton J. H. 1985; Stimulation of 1,2-diacylglycerol accumulation in hepatocytes by vasopressin, epinephrine, and angiotensin II. J Biol Chem 260:14201–14207
     [Google Scholar]
  4. Bok J. W., Silverman-Gavrila L. B., Lew R. R., Sone T., Bowring F. J., Catcheside D. E. A., Griffiths A. J. F. 2001; Structure and function analysis of the calcium-related gene spray in Neurospora crassa . Fungal Genet Biol 32:145–158
     [Google Scholar]
  5. Camacho L., Parton R., Trewavas A. J., Malho R. 2000; Imaging cytosolic free-calcium distribution and oscillations in pollen tubes with confocal microscopy: a comparison of different dyes and loading methods. Protoplasma 212:162–173
     [Google Scholar]
  6. Collinge A. J., Trinci A. P. J. 1974; Hyphal tips of wild-type and spreading colonial mutants of Neurospora crassa . Arch Microbiol 99:353–368
     [Google Scholar]
  7. Crank J. 1975 The Mathematics of Diffusion , 2nd edn. p  13 Oxford: Clarendon Press;
  8. Dicker J. W., Turian G. 1990; Calcium deficiencies and apical hyperbranching in wild-type and ‘frost’ and ‘spray’ morphological mutants of Neurospora crassa. J Gen Microbiol 136:1413–1420
     [Google Scholar]
  9. Dickman M. B., Yarden O. 1999; Serine/threonine protein kinases and phosphatases in filamentous fungi. Fungal Genet Biol 26:99–117
     [Google Scholar]
  10. Felle H. H., Hepler P. K. 1997; The cytosolic Ca2+ concentration gradient of Sinapsis alba root hairs as revealed by Ca2+-selective microelectrode tests and fura-dextran ratio imaging. Plant Physiol 114:39–45
     [Google Scholar]
  11. Fox D. S., Heitman J. 2002; Good fungi gone bad: the corruption of calcineurin. Bioessays 24:894–903
     [Google Scholar]
  12. Garrill A., Jackson S. L., Lew R. R., Heath I. B. 1993; Ion channel activity and tip growth: tip-localized, stretch-activated channels generate a Ca2+ gradient that is required for tip growth in the oomycete Saprolegnia ferax . Eur J Cell Biol 60:358–365
     [Google Scholar]
  13. Gooday G. W. 1971; An autoradiographic study of hyphal growth of some fungi. J Gen Microbiol 67:125–133
     [Google Scholar]
  14. Gorovits R., Propheta O., Kolot M., Dombradi V., Yarden O. 1999; A mutation within the catalytic domain of COT1 kinase confers changes in the presence of two COT1 isoforms and in Ser/Thr protein kinase and phosphatase activities in Neurospora crassa . Fungal Genet Biol 27:264–274
     [Google Scholar]
  15. Gupta G. D., Heath I. B. 2000; A tip-high gradient of a putative plasma membrane SNARE approximates the exocytotic gradient in hyphal apices of the fungus Neurospora crassa . Fungal Genet Biol 29:187–199
     [Google Scholar]
  16. Gupta G. D., Heath I. B. 2002; Predicting the distribution, conservation, and functions of SNAREs and related proteins in fungi. Fungal Genet Biol 36:1–21
     [Google Scholar]
  17. Ha K. S., Thompson G. A. Jr 1991; Diacylglycerol metabolism in the green alga Dunaliela salina under osmotic stress. Possible role of diacylglycerols in phospholipase C-mediated signal transduction. Plant Physiol 97:921–927
     [Google Scholar]
  18. Halachmi D., Eilam Y. 1993; Calcium homeostasis in yeast cells exposed to high concentrations of calcium. Roles of vacuolar H+-ATPase and cellular ATP. FEBS Lett 18:73–78
     [Google Scholar]
  19. Hall J. E., Simon A. 1976; A simple model for calcium induced exocytosis. Biochim Biophys Acta 436:613–616
     [Google Scholar]
  20. Hyde G. J., Heath I. B. 1997; Ca2+ gradients in hyphae and branches of Saprolegnia ferax . Fungal Genet Biol 21:238–251
     [Google Scholar]
  21. Jackson S. L., Heath I. B. 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]
  22. Kinnunen P. J. K. 2000; Lipid bilayers as osmotic response elements. Cell Physiol Biochem 10:243–250
     [Google Scholar]
  23. Kost B., Lemichez E., Spielhofer P., Hong Y., Tolias K., Carpenter C., Chua N.-H. 1999; Rac homologues and compartmentalized phosphatidylinositol 4,5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 145:317–330
     [Google Scholar]
  24. Levina N. N., Lew R. R., Hyde G. J., Heath I. B. 1995; The roles of Ca2+ and plasma membrane ion channels in hyphal tip growth of Neurospora crassa . J Cell Sci 108:3405–3417
     [Google Scholar]
  25. Lew R. R. 1999; Comparative analysis of Ca2+ and H+ flux magnitude and location along growing hyphae of Saprolegnia ferax and Neurospora crassa . Eur J Cell Biol 78:892–902
     [Google Scholar]
  26. Messerli M. A., Robinson K. R. 1997; Tip localized Ca2+ pulses are coincident with peak pulsatile growth rates in pollen tubes of Lilium longiflorum . J Cell Sci 110:1269–1278
     [Google Scholar]
  27. Messerli M. A., Danuser G., Robinson K. R. 1999; Pulsatile influxes of H+, K+ and Ca2+ lag growth pulses of Lilium longiflorum pollen tubes. J Cell Sci 112:1497–1509
     [Google Scholar]
  28. Messerli M. A., Creton R., Jaffe L. F., Robinson K. R. 2000; Periodic increases in elongation rate precede increases in cytosolic Ca2+ during pollen tube growth. Dev Biol 222:84–98
     [Google Scholar]
  29. Nakatani K., Chen C., Koutalos Y. 2002; Calcium diffusion coefficient in rod photoreceptor outer segments. Biophys J 82:728–739
     [Google Scholar]
  30. Ortega-Perez R., Irminger-Finger I., Arrighi J. F., Capelli N., van Tuinen D., Turian G. 1994; Identification and partial purification of calmodulin-binding microtubule-associated proteins from Neurospora crassa . Eur J Biochem 226:303–310
     [Google Scholar]
  31. Osherov N., May G. S. 2001; The molecular mechanism of conidial germination. FEMS Microbiol Lett 199:153–160
     [Google Scholar]
  32. Pierson E. S., Miller D. D., Calahan D. A., Shipley A. M., Rivers B. A., Cresti M., Hepler P. K. 1994; Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media. Plant Cell 6:1815–1828
     [Google Scholar]
  33. Pierson E. S., Miller D. D., Callahan D. A., van Aken J., Hackett G., Hepler P. K. 1996; Tip-localized calcium entry fluctuates during pollen tube growth. Dev Biol 174:160–173
     [Google Scholar]
  34. Prokisch H., Yarden O., Dieminger M., Tropschug M., Barthelmess I. B. 1997; Impairment of calcineurin function in Neurospora crassa reveals its essential role in hyphal growth, morphology and maintenance of the apical Ca2+ gradient. Mol Gen Genet 256:104–114
     [Google Scholar]
  35. Pu R., Robinson K. R. 1998; Cytoplasmic calcium gradients and calmodulin in the early development of the fucoid alga Pelvetia compressa. J Cell Sci 111:3197–3207
     [Google Scholar]
  36. Ramsdale M., Lakin-Thomas P. L. 2000; sn-1,2-Diacylglycerol levels in the fungus Neurospora crassa display circadian rhythmicity. J Biol Chem 275:27541–27550
     [Google Scholar]
  37. Rasband W. S., Bright D. 1995; NIH Image: a public domain image processing program for the Macintosh. Microbeam Anal Soc J 4:137–149
     [Google Scholar]
  38. Robson G. D., Wiebe M. G., Trinci A. P. J. 1991; Low calcium concentrations induce increased branching in Fusarium graminearum . Mycol Res 95:561–565
     [Google Scholar]
  39. Schiefelbein J. W., Shipley A., Rowse P. 1992; Calcium influx at the tip of growing root hairs of Arabidopsis thaliana . Planta 197:455–459
     [Google Scholar]
  40. Schmid J., Harold F. M. 1988; Dual roles for calcium ions in apical growth of Neurospora crassa . J Gen Microbiol 134:2623–2631
     [Google Scholar]
  41. Silverman-Gavrila L. B., Lew R. R. 2000; Calcium and tip growth in Neurospora crassa . Protoplasma 213:203–217
     [Google Scholar]
  42. Silverman-Gavrila L. B., Lew R. R. 2001; Regulation of the tip-high [Ca2+] gradient in growing hyphae of the fungus Neurospora crassa . Eur J Cell Biol 80:379–390
     [Google Scholar]
  43. Silverman-Gavrila L. B., Lew R. R. 2002; An IP3-activated Ca2+ channel regulates fungal tip growth. J Cell Sci 115:5013–5025
     [Google Scholar]
  44. Smith G. D., Keizer J. E., Stern M. D., Lederer W. J., Cheng H. 1998; A simple numerical model of calcium spark formation and detection in cardiac myocytes. Biophys J 75:15–32
     [Google Scholar]
  45. Suresh K., Subramanyam C. 1997; A putative role for calmodulin in the activation of Neurospora crassa chitin synthase. FEMS Microbiol Lett 150:95–100
     [Google Scholar]
  46. Tanaka Y., Hata S., Ishiro H., Ishii K., Nakayama K. 1994; Quick stretch increases the production of inositol 1,4,5-trisphosphate (IP3) in porcine coronary artery. Life Sci 55:227–235
     [Google Scholar]
  47. Tellez-Inon M. T., Ulloa R. M., Glikin G. C., Torres H. N. 1985; Characterization of Neurospora crassa cyclic AMP phosphodiesterase activated by calmodulin. Biochem J 232:425–430
     [Google Scholar]
  48. Torralba S., Heath I. B. 2001; Cytoskeletal and Ca2+ regulation of hyphal tip growth and initiation. Curr Top Dev Biol 51:135–187
     [Google Scholar]
  49. Torralba S., Heath I. B., Ottensmeyer F. P. 2001; Ca2+ shuttling in vesicles during tip growth in Neurospora crassa . Fungal Genet Biol 33:181–193
     [Google Scholar]
  50. Turner B. C., Perkins D. D., Fairfield A. 2001; Neurospora from natural populations: a global study. Fungal Genet Biol 32:67–92
     [Google Scholar]
  51. Vogel H. J. 1956; A convenient growth medium for Neurospora . Microb Genet Bull 13:42–46
     [Google Scholar]
  52. Wang J. H. 1953; Tracer-diffusion in liquids. IV. Self-diffusion of calcium ion and chloride ion in aqueous calcium chloride solutions. J Am Chem Soc 75:1769–1770
     [Google Scholar]
  53. Wilkinson L. 1988 systat: The System for Statistics Evanston, IL: SYSTAT;
  54. Wymer C. L., Bibikova T. N., Gilroy S. 1997; Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana . Plant J 12:427–439
     [Google Scholar]
  55. Yin H. L., Janmey P. A. 2003; Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 65:761–789
     [Google Scholar]
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Calcium gradient dependence of Neurospora crassa hyphal growth
Microbiology 149, 2475 (2003); https://doi.org/10.1099/mic.0.26302-0
/content/journal/micro/10.1099/mic.0.26302-0
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