1887

Abstract

Movement of nuclei, mitochondria and vacuoles through hyphal trunks of were vector-mapped using fluorescent markers and green fluorescent protein tags. The vectorial movements of all three were strongly correlated, indicating the central role of mass (bulk) flow in cytoplasm movements in . Profiles of velocity versus distance from the hyphal wall did not match the parabolic shape predicted by the ideal Hagen–Poiseuille model of flow at low Reynolds number. Instead, the profiles were flat, consistent with a model of partial plug flow due to the high concentration of organelles in the flowing cytosol. The intra-hyphal pressure gradients were manipulated by localized external osmotic treatments to demonstrate the dependence of velocity (and direction) on pressure gradients within the hyphae. The data support the concept that mass transport, driven by pressure gradients, dominates intra-hyphal transport. The transport occurs by partial plug flow due to the organelles in the cytosol.

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2013-11-01
2020-01-24
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References

  1. Bebber D. P., Hynes J., Darrah P. R., Boddy L., Fricker M. D..( 2007;). Biological solutions to transport network design. Proc Biol Sci274:2307–2315 [CrossRef][PubMed]
    [Google Scholar]
  2. Bleichrodt R., Vinck A., Krijgsheld P., van Leeuwen M. R., Dijksterhuis J., Wösten H. A..( 2013;). Cytosolic streaming in vegetative mycelium and aerial structures of Aspergillus niger. Stud Mycol74:31–46 [CrossRef][PubMed]
    [Google Scholar]
  3. Bowman B. J., Draskovic M., Freitag M., Bowman E. J..( 2009;). Structure and distribution of organelles and cellular location of calcium transporters in Neurospora crassa. Eukaryot Cell8:1845–1855 [CrossRef][PubMed]
    [Google Scholar]
  4. Cox R. G., Mason S. G..( 1971;). Suspended particles in fluid flow through tubes. Annu Rev Fluid Mech3:291–316 [CrossRef]
    [Google Scholar]
  5. Darrah P. R., Tlalka M., Ashford A., Watkinson S. C., Fricker M. D..( 2006;). The vacuole system is a significant intracellular pathway for longitudinal solute transport in basidiomycete fungi. Eukaryot Cell5:1111–1125 [CrossRef][PubMed]
    [Google Scholar]
  6. Esseling-Ozdoba A., Houtman D., VAN Lammeren A. A. M., Eiser E., Emons A. M. C..( 2008;). Hydrodynamic flow in the cytoplasm of plant cells. J Microsc231:274–283 [CrossRef][PubMed]
    [Google Scholar]
  7. Freitag M., Hickey P. C., Raju N. B., Selker E. U., Read N. D..( 2004;). GFP as a tool to analyze the organization, dynamics and function of nuclei and microtubules in Neurospora crassa. Fungal Genet Biol41:897–910 [CrossRef][PubMed]
    [Google Scholar]
  8. Fricker M. D., Lee J. A., Bebber D. P., Tlalka M., Hynes J., Darrah P. R., Watkinson S. C., Boddy L..( 2008;). Imaging complex nutrient dynamics in mycelial networks. J Microsc231:317–331 [CrossRef][PubMed]
    [Google Scholar]
  9. Jennings D. H..( 1987;). Translocation of solutes in fungi. Biol Rev Camb Philos Soc62:215–243 [CrossRef]
    [Google Scholar]
  10. Jensen K. H., Lee J., Bohr T., Bruus H..( 2009;). Osmotically driven flows in microchannels separated by a semipermeable membrane. Lab Chip9:2093–2099 [CrossRef][PubMed]
    [Google Scholar]
  11. Karnis A., Goldsmith H. L., Mason S. G..( 1966;). The kinetics of flowing dispersions. I. Concentrated suspensions of rigid particles. J Colloid Interface Sci22:531–553 [CrossRef]
    [Google Scholar]
  12. Knoblauch M., Peters W. S..( 2010;). Münch, morphology, microfluidics – our structural problem with the phloem. Plant Cell Environ33:1439–1452[PubMed]
    [Google Scholar]
  13. Levina N. N., Lew R. R..( 2006;). The role of tip-localized mitochondria in hyphal growth. Fungal Genet Biol43:65–74 [CrossRef][PubMed]
    [Google Scholar]
  14. Lew R. R..( 2005;). Mass flow and pressure-driven hyphal extension in Neurospora crassa. Microbiology151:2685–2692 [CrossRef][PubMed]
    [Google Scholar]
  15. Lew R. R..( 2011;). How does a hypha grow? The biophysics of pressurized growth in fungi. Nat Rev Microbiol9:509–518 [CrossRef][PubMed]
    [Google Scholar]
  16. Lew R. R., Nasserifar S..( 2009;). Transient responses during hyperosmotic shock in the filamentous fungus Neurospora crassa. Microbiology155:903–911 [CrossRef][PubMed]
    [Google Scholar]
  17. Luck D. J. L..( 1963;). Formation of mitochondria in Neurospora crassa. A quantitative radioautographic study. J Cell Biol16:483–499 [CrossRef][PubMed]
    [Google Scholar]
  18. McCluskey K., Wiest A., Plamann M..( 2010;). The Fungal Genetics Stock Center: a repository for 50 years of fungal genetics research. J Biosci35:119–126 [CrossRef][PubMed]
    [Google Scholar]
  19. Pickard W. F..( 2006;). Absorption by a moving spherical organelle in a heterogeneous cytoplasm: implications for the role of trafficking in a symplast. J Theor Biol240:288–301 [CrossRef][PubMed]
    [Google Scholar]
  20. Ramos-García S. L., Roberson R. W., Freitag M., Bartnicki-García S., Mouriño-Pérez R. R..( 2009;). Cytoplasmic bulk flow propels nuclei in mature hyphae of Neurospora crassa. Eukaryot Cell8:1880–1890 [CrossRef][PubMed]
    [Google Scholar]
  21. Rasband W. S..( 2013;). U. S. National Institutes of Health; Bethesda, Maryland, USA:http://imagej.nih.gov/ij/
  22. Riquelme M., Roberson R. W., McDaniel D. P., Bartnicki-García S..( 2002;). The effects of ropy-1 mutation on cytoplasmic organization and intracellular motility in mature hyphae of Neurospora crassa. Fungal Genet Biol37:171–179 [CrossRef][PubMed]
    [Google Scholar]
  23. Roper M., Simonin A., Hickey P. C., Leeder A., Glass N. L..( 2013;). Nuclear dynamics in a fungal chimera. Proc Natl Acad Sci U S A110:12875–12880 [CrossRef][PubMed]
    [Google Scholar]
  24. Simonin A., Palma-Guerrero J., Fricker M., Glass N. L..( 2012;). Physiological significance of network organization in fungi. Eukaryot Cell11:1345–1352 [CrossRef][PubMed]
    [Google Scholar]
  25. Steinberg G..( 2007;). Hyphal growth: a tale of motors, lipids, and the Spitzenkörper. Eukaryot Cell6:351–360 [CrossRef][PubMed]
    [Google Scholar]
  26. Verchot-Lubicz J., Goldstein R. E..( 2010;). Cytoplasmic streaming enables the distribution of molecules and vesicles in large plant cells. Protoplasma240:99–107 [CrossRef][PubMed]
    [Google Scholar]
  27. Vogel H. J..( 1956;). A convenient growth medium for Neurospora. Microbial Genetics Bulletin13:42–46
    [Google Scholar]
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