Cell-to-Cell Communication in the Tip Growth of Mycelial Fungi

Chapter

Abstract

The capacity of fungi to explore solid substrate, invade tissues and secrete digestive enzymes are all linked to their particular mode of growth, extension of a tip. The high rate of tip growth provide by the coordinated activity dozens of cells having the septal pores allowing ions, molecules and organelles move along the hyphae. Young apical cells are deficient to generate a potential difference across the plasma membrane. For this reason, in the apical area of about 300 μm a significant electric field (100 V/m) appears and strong intercellular current flows (some nanoA). Perhaps this electrical heterogeneity plays an important role in the self-organization of interactions between cells and intracellular structures in the tip growth.

Keywords

Neurospora crassa Tip growth Movement of mitochondria Intercellular electrical currents 

References

  1. Alekseevskii AV, Belozerskaya TA, Boitzova LJu, Lukina EN, Potapova TV, Toms KS (1999) New approaches to analysis of characteristics of self-organization of multicellular systems during polarized apical growth. Dokl Biophys 369:108–111Google Scholar
  2. Aslanidi KB, Potapova TV, Shalapjenok AA, Karnauhov VN, Chailakhyan LM (1986) Photoelectric activity and spectral parameters of the unit trichome of Phormidium uncinatum. Dokladi Akademii Nauk SSSR 290:1504–1507 (in Russian)Google Scholar
  3. Aslanidi KB, Potapova TV, Chailakhyan LM (1988) Energy transmission through the high permeable intercellular junctions. Biol Membrany 5:613–627 (in Russian)Google Scholar
  4. Aslanidi KB, Boitzova LJu, Chailakhyan LM, Kublik LN, Marachova II, Moch VN, Potapova TV, Trepakova EK, Vinogradova TN (1991) Maintenance of ion-osmotic homeostasis in multicellular animal systems: the role of permeable junctions. Biol Membrany 8:837–853 (in Russian)Google Scholar
  5. Aslanidi KB, Boitzova LJu, Potapova TV, Smolianinov VV (1996) Information-energy module as the functional unit of the Neurospora crassa polarized growth. Membr Cell Biol (Russia) 10:27–37Google Scholar
  6. Aslanidi KB, Aslanidi OV, Vachadze DM, Mornev OA, Potapova TV, Chailakhyan LM, Shtemanetian EG (1997) Analysis of electrical phenomena accompanying the growth of Neurospora crassa hyphae: theory and experiment. Membr Cell Biol (Russia) 11:349–365Google Scholar
  7. Aslanidi KB, Pogorelov FG, Aslanidi OV, Mornev OA, Potapova TV (2000) The distribution of potassium in Neurospora crassa hyphae. Doklady Russ Acad Sci 372:253–256 (in Russian)Google Scholar
  8. Belozerskaya TA, Potapova TV (1993) Intrahyphal communication in segmented mycelium. Exp Mycol 17:157–169CrossRefGoogle Scholar
  9. Bereihter-Hahn J (1990) Behavior of mitochondria in the living cell. Int Rev Cytol 122:1–63CrossRefGoogle Scholar
  10. Böhm KJ, Nikolaos E, Mavromatos NE, Michette A, Stracke R, Unger E (2005) Movement and alignment of microtubules in electric fields and electric-dipole-moment estimates. Electromagn Biol Med 24:319–330CrossRefGoogle Scholar
  11. Borkovich KA, Alex LA, Yarden O, Freitag M et al (2004) Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev 68:1–108PubMedCrossRefGoogle Scholar
  12. Caldwell JY, Trinci APJ (1973) The growth unit of the mould Geotrichum candidum. Arch Microbiol 88:1–10Google Scholar
  13. Chada SR, Hollenbeck PJ (2003) Mitochondrial movement and positioning in axons: the role of growth factor signalling. J Exp Biol 206:1985–1992PubMedCrossRefGoogle Scholar
  14. Chailakhyan LM, Glagolev AN, Glagoleva TN, Murvanidze GM, Potapova TV, Skulachev VP (1982) Intercellular power transmission along trichomes of cyanobacteria. Biochem Biophys Acta 679:60–73CrossRefGoogle Scholar
  15. Chailakhyan LM, Potapova TV, Levina NN, Belozerskaya TA, Kritzky MS (1985) A study of intercellular communication in Neurospora crassa with special reference to photoelectric responses of membranes. Biol Membrany 1:76–101 (in Russian)Google Scholar
  16. Collinge AJ, Trinci APJ (1974) Hyphal tips of wild-type and spreading colonial mutants of Neurospora crassa. Arch Microbiol 99:353–368PubMedCrossRefGoogle Scholar
  17. Davis RH (2000) Neurospora: contributions of a model organism. Oxford University Press, OxfordGoogle Scholar
  18. Dujovne I, van den Heuvel M, Shen Y, de Graaff M, Dekker C (2008) Velocity modulation of microtubules in electric fields. Nano Lett 8:4217–4220PubMedCrossRefGoogle Scholar
  19. Fischer R, Zekert N, Takeshita N (2008) Polarized growth in fungi – interplay between the cytoskeleton, positional markers and membrane domains. Mol Microbiol 68:813–826PubMedCrossRefGoogle Scholar
  20. Fuchs F, Westermann B (2005) Role of Unc104/KIF1-related motor proteins in mitochondrial transport in Neurospora crassa. Mol Biol Cell 16:153–161PubMedCrossRefGoogle Scholar
  21. Gow NAR (1989) Circulating ionic currents in micro-organisms. Adv Microb Physiol 30:90–123Google Scholar
  22. Gow NAR, Kropf DL, Harold FM (1984) Growing hyphae of Achlya bisexualis generate a longitudinal pH gradient in the surrounding media. J Gen Microbiol 130:2967–2974PubMedGoogle Scholar
  23. Gradmann D, Hansen U-P, Long WS, Slayman CL, Warncke J (1978) Current–voltage relationships for the plasma membrane and its principal electrogenic pump in Neurospora crassa. J Membr Biol 39:333–367PubMedCrossRefGoogle Scholar
  24. Harold FM (1986) The vital force: a study of bioenergetics. Freeman and Co., New YorkGoogle Scholar
  25. Harold FM (1994) Ionic and electrical dimensions of hyphal growth. In: Wessels JGH, Meinhardt F (eds) The mycota I. Growth, differentiation and sexuality. Springer, Berlin/Heidelberg, pp 89–109Google Scholar
  26. Harold FM (2001) The way of the cell: molecules, organisms and the order of life. Oxford University Press, OxfordGoogle Scholar
  27. Harold FM, Caldwell JH (1990) Tips and currents: electrobiology of apical growth. In: Heath IB (ed) Tip growth in plant and fungal cells. Academic Press Inc., Orlando/San Diego, pp 59–90Google Scholar
  28. Haugland RP (2002) Handbook of fluorescent probes, 9th edn. Molecular Probes, EugeneGoogle Scholar
  29. Held M, Edwards C, Nicolau DV (2010) Temporal and spatial in vivo optical analysis of microtubules in Neurospora crassa. In: Farkas DL, Nicolau DV, Leif RC (eds) Imaging, manipulation, and analysis of biomolecules, cells, and tissues VIII. SPIE, San Francisco, p 75680VGoogle Scholar
  30. Hickey PC, Swift SR, Roca MG, Read ND (2005) Live-cell imaging of filamentous fungi using vital fluorescent dyes and confocal microscopy. Methods Microbiol 34:63–87CrossRefGoogle Scholar
  31. Jaffe LF, Nuccitelli R (1974) An ultrasensitive vibrating probe for measuring steady extracellular currents. J Cell Biol 63:614–628PubMedCrossRefGoogle Scholar
  32. Jaffe LF, Nuccitelli R (1977) Electrical control of development. Annu Rev Biophys Bioeng 6:445–476PubMedCrossRefGoogle Scholar
  33. Kropf DL (1986) Electrophysiological study of Achlea hyphae: ionic currents studied by intracellular potential recording. J Cell Biol 102:1209–1216PubMedCrossRefGoogle Scholar
  34. Kropf DL, Caldwell JH, Gow NAR, Harold FM (1984) Transcellular ion currents in the water mold Achlea: amino acid proton symport as a mechanism of current entry. J Cell Biol 99:86–96CrossRefGoogle Scholar
  35. Levina NN, Lew RR (2006) The role of tip-localized mitochondria in hyphal growth. Fungal Genet Biol 43:65–74PubMedCrossRefGoogle Scholar
  36. Lew RR (1999) Comparative analysis of Ca and H flux magnitude and location along growing hyphae of Saprolegnia ferax and Neurospora crassa. Eur J Cell Biol 78:892–902PubMedCrossRefGoogle Scholar
  37. Lew RR, Levina NN (2004) Oxygen flux magnitude and location along growing hyphae of Neurospora crassa. FEMS Microbiol Lett 233:125–130PubMedCrossRefGoogle Scholar
  38. Loewenstein WR (1981) Junctional intercellular communication: the cell-to-cell membrane channel. Physiol Rev 61:829–913PubMedGoogle Scholar
  39. Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144–148PubMedCrossRefGoogle Scholar
  40. Mitchell P (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol Rev Camb Philos Soc 41:445–502PubMedCrossRefGoogle Scholar
  41. Potapova TV, Aslanidi KB (1995) Energy coupling of adjacent cells as an universal function of cell-to-cell permeable junctions. In: Kanno Y (ed) Intercellular communication through gap junctions, Progress in cell res 4. Elsevier Science B.V., Amsterdam, pp 53–56Google Scholar
  42. Potapova TV, Boitzova LJu (1998) Structure, function, regulation: experimental analysis in groups of non-excitable cells coupled via permeable junctions. Membr Cell Biol (Russia) 11:817–829Google Scholar
  43. Potapova TV, Levina NN (1985) Reactions of Neurospora to a local lesion of the cell membrane. Biol Membrany 2:123–127 (in Russian)Google Scholar
  44. Potapova TV, Aslanidi KB, Belozerskaya TA, Levina NN (1988) Transcellular ionic currents studied by intracellular potential recordings in Neurospora crassa hyphae. (Transfer of energy from proximal to apical cells). FEBS Lett 241:173–176PubMedCrossRefGoogle Scholar
  45. Potapova TV, Aslanidi KB, Boitzova LJu (1990) Energy transfer via cell-to-cell junctions: ouabain-resistant cells maintain a membrane potential in ouabain-sensitive cells. FEBS Lett 262:69–71PubMedCrossRefGoogle Scholar
  46. Potapova TV, Boytzova LJu, Alexeevskii AV, Smoljaninov VV (2001) The functional role of intercellular interactions at the Neurospora crassa hyphae: influence of distant mycelium part on the tip growth. Biol Membrany 18:364–369 (in Russian)Google Scholar
  47. Potapova TV, Boytzova LJu, Alexeevskii AV, Smoljaninov VV, Belozerskaya TA (2003) Tip growth of the genetically different Neurospora crassa strains: effects of electrical isolation and nitrogen depletion. Biol Membrany 20:395–400 (in Russian)Google Scholar
  48. Potapova TV, Alexeevskii TA, Boitzova LJu (2008) Tip growth of Neurospora during glucose deprivation. Membr Cell Biol (Russia) 25:171–177Google Scholar
  49. Potapova TV, Boitzova LJu, Golyshev SA, Popinako AV (2011) Dynamics of mitochondria during Neurospora crassa tip growth. Membr Cell Biol (Russia) 28:345–353Google Scholar
  50. Riquelme M, Robetson RW, McDaniel DP, Bartnicki-Garcia S (2002) The effect of ropy-1 mutation on cytoplasmic organization and intracellular motility in mature hyphae of Neurospora crassa. Fungal Genet Biol 37:171–179PubMedCrossRefGoogle Scholar
  51. Rodriquez-Navarro A (1986) A potassium-proton symport in Neurospora crassa. J Gen Physiol 87:649–674CrossRefGoogle Scholar
  52. Sanders D, Slayman CL, Pall ML (1983) Stoichiometry of H+/amino acid cotransport in Neurospora crassa revealed by current–voltage analysis. Biochim Biophys Acta 735:67–76PubMedCrossRefGoogle Scholar
  53. Silverman-Gavrila LB, Lew RR (2003) Calcium gradient dependence of Neurospora crassa hyphal growth. Microbiology 149:2475–2485PubMedCrossRefGoogle Scholar
  54. Slayman CL (1987) The plasma membrane potential of Neurospora crassa: a proton pumping electroenzyme. J Bioenerg Biomembr 19:1–20PubMedGoogle Scholar
  55. Slayman CL, Slayman CW (1974) Depolarization of the plasma membrane of Neurospora crassa during active transport of glucose. Proc Natl Acad Sci USA 71:1931–1939CrossRefGoogle Scholar
  56. Slayman CL, Long WS, Lu CY-H (1973) The relationship between ATP and an electrogenic pump in the plasma membrane of Neurospora crassa. J Membr Biol 14:305–338PubMedCrossRefGoogle Scholar
  57. Smolyaninov VV, Potapova TV (2003) Evaluation of the critical fragment length of Neurospora crassa hyphae. Biol Membrany 20:314–321 (in Russian)Google Scholar
  58. Steinberg G (2007) Hyphal growth: a tale of motors, lipids, and spitzenkorper. Eukaryot Cell 6:351–360PubMedCrossRefGoogle Scholar
  59. Steinberg G, Schliwa M (1993) Organelle movements in the wild type and wall-less fz; sg; os-1 mutants of Neurospora crassa are mediated by cytoplasmic microtubules. J Cell Sci 106:555–564PubMedGoogle Scholar
  60. Sugden KEP, Evans MR, Poon WCK, Read ND (2007) Model of hyphal tip growth involving microtubule-based transport. Phys Rev E 75:031909CrossRefGoogle Scholar
  61. Takeuchi G, Schmidt J, Caldwell JH, Harold FM (1988) Transcellular ion currents and extension of Neurospora crassa hyphae. J Membr Biol 101:33–41PubMedCrossRefGoogle Scholar
  62. Tey WK, North AJ, Reyes JL, Lu YF, Jedd G (2005) Polarized gene expression determines Woronian body formation at the leading edge of the fungal colony. Mol Biol Cell 16:2651–2659PubMedCrossRefGoogle Scholar
  63. Trinci APJ, Wiebe MG, Robson GD (1994) The mycelium as an integrated entity. In: Wessels JGH, Meinhart F (eds) The mycota I. Growth, differentiation and sexuality. Springer, Berlin/Heidelberg, pp 175–193Google Scholar
  64. Westermann B (2008) Molecular machinery of mitochondrial fusion and fission. J Biol Chem 283:13501–13505PubMedCrossRefGoogle Scholar
  65. Yaffe MP (1999) The machinery of mitochondrial inheritance and behavior. Science 283:1493–1497PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  1. 1.Belozersky Institute of Physicochemical BiologyMoscow Lomonosov State UniversityMoscowRussia

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