Protoplasma

, Volume 191, Issue 1–2, pp 105–114

Growth and morphogenesis inSaprolegnia ferax: Is turgor required?

  • Ruth L. Harold
  • N. P. Money
  • F. M. Harold
Article

Summary

The oomyceteSaprolegnia ferax, unlike most walled organisms, does not regulate turgor. When hyphae were subjected to water stress by the addition of sucrose or other solutes to the growth medium, turgor pressure diminished progressively; yet the hyphae continued to extend with deposition of a more plastic apical wall. Even when turgor was no longer measurable with a micropipet-based pressure probe (0.02 MPa or less, compared with 0.4 MPa in unsupplemented medium) they produced regular hyphal tubes and tips. Such “turgorless” hyphae extended as rapidly, or more rapidly, than normal ones, but they were wider and their tips blunter. Despite the loss of turgor, hyphae put forth branches and cysts germinated. The organization of actin microfilaments was essentially normal, and the response to cytochalasin A was similar in turgorless and standard hyphae. However, as turgor diminished the hyphae's capacity to penetrate solid media was progressively impaired; aerial hyphae were no longer produced, and zoospore formation was inhibited. The results contradict the common belief that turgor supplies the driving force for hyphal extension, tip morphogenesis, and branching. Evidently, these functions do not intrinsically require hydrostatic pressure. Turgorless hyphae are, however, crippled by their inability to exploit solid media.

Keywords

Turgor Hydrostatic pressure Apical growth Tip growth Saprolegnia ferax 

Abbreviations

PEG-300

polyethylene glycol-300

Rh-Phal

rhodamine phalloidin

F-actin

filamentous actin

DMSO

dimethyl sulfoxide

PYG

peptone, yeast extract, glucose

MPa

megapascals

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References

  1. Adebayo AA, Harris RF, Gardner WR (1971) Turgor pressure of fungal mycelia. Trans Br Mycol Soc 57: 145–151Google Scholar
  2. Ariztia EV, Andersen RA, Sogin ML (1991) A new phylogeny for chromophyte algae using 16S-like rRNA sequences fromMallomonas papillosa (Synurophyceae) andTribonema aequale (Xanthophyceae). J Phycol 27: 428–436Google Scholar
  3. Cooper JA (1987) Effects of cytochalasin and phalloidin on actin. J Cell Biol 105: 1473–1478Google Scholar
  4. Cosgrove DJ (1986) Biophysical control of plant cell growth. Annu Rev Plant Physiol 37: 377–405Google Scholar
  5. — (1993) How do plant cells extend? Plant Physiol 102: 1–6Google Scholar
  6. Duniway JM (1979) Water relations of water molds. Annu Rev Phytopathol 17: 431–460Google Scholar
  7. Eamus D, Jennings DH (1986) Water, turgor, and osmotic potentials of fungi. In: Ayres PG, Boddy L (eds) Water, fungi and plants. Cambridge University Press, Cambridge, pp 27–48Google Scholar
  8. Green PB, Stanton FW (1967) Turgor pressure: direct manometric measurement in single cells ofNitella. Science 155: 1675–1676Google Scholar
  9. Griffin DM (1994) Fungal physiology, 2nd edn. Wiley Liss, New YorkGoogle Scholar
  10. Gubler F, Hardham AR, Dumiec J (1989) Characterizing adhesiveness ofPhytophthora cinnamomi zoospores during encystment. Protoplasma 149: 24–30Google Scholar
  11. Gunderson JH, Elwood H, Ingold A, Kindle K, Sogin ML (1987) Phylogenetic relationships between chlorophytes, chrysophytes and oomycetes. Proc Natl Acad Sci USA 84: 5823–5827Google Scholar
  12. Hardegree SP, Emmerich WE (1990) Effect of polyethylene glycol exclusion on the water potential of solution-saturated filter paper. Plant Physiol 92: 462–466Google Scholar
  13. Harold FM (1990) To shape a cell: an inquiry into the causes of morphogenesis of microorganisms. Microbiol Rev 54: 381–431Google Scholar
  14. Harold RL, Harold FM (1986) Ionophores and cytochalasins modulate branching inAchlya bisexualis. J Gen Microbiol 132: 213–219Google Scholar
  15. — — (1992) Configuration of actin microfilaments during sporangium development inAchlya bisexualis: a comparison of two staining protocols. Protoplasma 171: 110–116Google Scholar
  16. Heath IB (1987) Preservation of a labile cortical array of actin filaments in growing hyphal tips of the fungusSaprolegnia ferax. Eur J Cell Biol 44: 10–16Google Scholar
  17. Heath IB (1990) The roles of actin in tip growth of fungi. Int Rev Cytol 123: 95–127Google Scholar
  18. —, Harold RL (1992) Actin has multiple roles in the formation and architecture of zoospores of the oomycetes,Saprolegnia ferax andAchlya bisexualis. J Cell Sci 102: 611–627Google Scholar
  19. Jackson SL, Heath IB (1990) Evidence that actin reinforces the extensible hyphal apex of the oomyceteSaprolegnia ferax. Protoplasma 157: 144–153Google Scholar
  20. Kaminskyj SGW, Garrill A, Heath IB (1992) The relation between turgor and tip growth inSaprolegnia ferax: turgor is necessary, but not sufficient to explain apical extension rates. Exp Mycol 16: 64–75Google Scholar
  21. Kelly S, Macklem PT (1991) Direct measurement of intracellular pressure. Am J Physiol 260: C652-C657Google Scholar
  22. Koch AL (1982) The shape of the hyphal tip of fungi. J Gen Microbiol 128: 947–951Google Scholar
  23. — (1985) How bacteria grow and divide in spite of internal hydrostatic pressure. Can J Microbiol 31: 1071–1083Google Scholar
  24. — (1994) The problem of hyphal growth in streptomycetes and fungi. J Theor Biol 171: 137–150Google Scholar
  25. Kropf DL, Caldwell JH, Gow NAR, Harold FM (1984) Transcellular ion currents in the water moldAchlya. Amino acid proton symport as a mechanism of current entry. J Cell Biol 99: 486–496Google Scholar
  26. Money NP (1989) Osmotic pressure of aqueous polyethylene glycols. Relationship between molecular weight and vapor pressure deficit. Plant Physiol 91: 766–769Google Scholar
  27. — (1990) Measurement of hyphal turgor. Exp Mycol 14: 416–425Google Scholar
  28. — (1994) Osmotic adjustment and the role of turgor in mycelial fungi. In: Meinhardt F, Wessels JGH (eds) The Mycota, vol 1. Springer, Berlin Heidelberg New York Tokyo, pp 67–88Google Scholar
  29. —, Harold FM (1992) Extension growth of the water moldAchlya: interplay of turgor and wall strength. Proc Natl Acad Sci USA 89: 4245–4249Google Scholar
  30. — — (1993) Two water molds can grow without measurable turgor pressure. Planta 190: 426–430Google Scholar
  31. Nobel PS (1983) Biophysical plant physiology and ecology. WH Freeman, New YorkGoogle Scholar
  32. Ray PM, Green PB, Cleland R (1972) Role of turgor in plant cell growth. Nature 239: 163–164Google Scholar
  33. Saunders PT, Trinci APJ (1979) Determination of tip shape in fungal hyphae. J Gen Microbiol 110: 469–473Google Scholar
  34. Schreurs WJA, Harold RL, Harold FM (1989) Chemotropism and branching as alternative responses ofAchlya bisexualis to amino acids. J Gen Microbiol 135: 2519–2528Google Scholar
  35. Steer MW (1990) Role of actin in tip growth. In: Heath IB (ed) Tip growth in plant and fungal cells. Academic Press, San Diego, pp 119–145Google Scholar
  36. Taiz L (1984) Plant cell expansion: regulation of cell wall mechanical properties. Annu Rev Plant Physiol 35: 585–657Google Scholar
  37. Thomas DDS, Mullins JT (1967) Role of enzymatic wall-softening in plant morphogenesis: hormonal induction inAchlya. Science 156: 84–85Google Scholar
  38. Trinci APJ (1978) Wall and hyphal growth. Sci Prog 65: 75–99Google Scholar
  39. Wessels JGH (1986) Cell wall synthesis in apical hyphal growth. Int Rev Cytol 104: 37–79Google Scholar
  40. — (1993) Wall growth, protein excretion and morphogenesis in fungi. New Phytol 123: 397–413Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • Ruth L. Harold
    • 1
  • N. P. Money
    • 2
  • F. M. Harold
    • 1
  1. 1.Department of Biochemistry and Molecular BiologyColorado State UniversityFort CollinsUSA
  2. 2.Department of BotanyMiami UniversityOxford

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