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UV microirradiation implicates F-actin in reinforcing growing hyphal tips

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Summary

The cell walls of plants and fungi are thought to provide the strength required to resist turgor and thus maintain the integrity and morphology of these cells. However, during growth, walls must undergo rapid expansion which requires them to be plastic and therefore weak. In most tip-growing cells there is an apical concentration of F-actin associated with the rapidly expanding cell wall. Disruption of F-actin in the growing tips of hyphae ofSaprolegnia ferax by a localized irradiation, beginning 2–6 μm behind the apex, with actin-selective 270 nm uv light caused the hyphae to burst, suggesting that actin supports the weak apical wall against turgor pressure. Bursting was pH dependent and Ca2+ independent at neutral pH. Hyphae burst in the very tip, where the cell wall is expected to be weakest and actin is most concentrated, as opposed to the lower part of the apical taper where osmotic shock induces bursting when actin is intact. When hyphae were irradiated with a wavelength of light that is less effective at disrupting actin, growth was slowed but they failed to burst, demonstrating that bursting was most likely due to F-actin damage. We conclude that F-actin reinforces the expanding apical wall in growing hyphae and may be the prime stress bearing structure resisting turgor pressure in tip growing cells.

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Abbreviations

RP:

rhodamine phalloidin

F-actin:

filamentous actin

EGTA:

ethylene-glycol-bis-(β-amino-ethyl ether) N,N′-tetra-acetic acid

PIPES:

piperazine-N,N′-bis-(2-ethanesulfonic acid)

uv:

ultraviolet

References

  • Adams AEM, Botstein D, Drubin DC (1989) A yeast actin-binding protein is encoded by SAC6, a gene found by suppression of an actin mutation. Science 243: 231–233

    PubMed  Google Scholar 

  • — — — (1991) Requirement of yeast fimbrin for actin organization and morphogenesis in vivo. Nature 354: 404–408

    PubMed  Google Scholar 

  • Bartnicki-Garcia S, Lippman E (1972) The bursting tendency of hyphal tips of fungi: presumptive evidence for a delicate balance between wall synthesis and wall lysis in apical growth. J Gen Microbiol 73: 487–500

    Google Scholar 

  • Bittisnich DJ, Williamson RE (1989) Tip-localised H+-fluxes and applicability of acid growth hypothesis to tip-growing cells: control of chloronemal extension inFunaria hygrometrica by auxin and light. Planta 178: 96–102

    Google Scholar 

  • Bretscher A (1981) Fimbrin is a cytoskeletal protein that crosslinks F-actin in vitro. Proc Natl Acad Sci USA 78: 6849–6853

    PubMed  Google Scholar 

  • Butt TM, Heath IB (1988) The changing distribution of actin and nuclear behavior during the cell cycle of the mite-pathogenic fungusNeozygites sp. Eur J Cell Biol 46: 499–505

    PubMed  Google Scholar 

  • Condeelis J, Vahey M, Carboni JM, DeMey J, Ogihara S (1984) Properties of the 120,000- and 95,000-dalton actin-binding proteins fromDictyostelium discoideum and their possible functions in assembling the cytoplasmic matrix. J Cell Biol 99: 119 s-126 s

    Google Scholar 

  • Czaban BB, Forer A (1991) Visualization of ultraviolet microbeam irradiation sites with uranyl acetate. J Microsc 164: 61–65

    Google Scholar 

  • Doonan JH, Cove DJ, Lloyd CW (1988) Microtubules and microfilaments in tip growth: evidence that microtubules impose polarity on protonemal growth inPhyscomitrella patens. J Cell Sci 89: 533–540

    Google Scholar 

  • Dow JM, Rubery PH (1975) Hyphal tip bursting inMucor rouxii: antagonistic effects of calcium ions and acid. J Gen Microbiol 91: 425–428

    PubMed  Google Scholar 

  • Drubin DG (1990) Actin and actin-binding proteins in yeast. Cell Motil Cytoskeleton 15: 7–11

    PubMed  Google Scholar 

  • Forer A (1991) In ultraviolet microbeam irradiations, characteristics of the monochromator and lamp affect the spectral composition of the ultra violet light and probably biological results. J Cell Sci 98: 415–422

    PubMed  Google Scholar 

  • Glenney JR, Kaulfus P, Matsudaira P, Weber K (1981) F-actin binding and bundling properties of fimbrin, a major cytoskeletal protein of microvillus core filaments. J Biol Chem 256: 9283–9288

    PubMed  Google Scholar 

  • 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: 10–16

    Google Scholar 

  • — (1990) The roles of actin in tip growth of fungi. Int Rev Cytol 123: 95–127

    Google Scholar 

  • —, Greenwood AD (1970) Centriole replication and nuclear division inSaprolegnia. J Gen Microbiol 62: 139–148

    Google Scholar 

  • —, Kaminskyj SGW (1989) The organization of tip-growth-related organelles and microtubules revealed by quantitative analysis of freeze-substituted oomycete hyphae. J Cell Sci 93: 41–52

    Google Scholar 

  • Hoch HC, Staples RC (1983) Visualization of actin in situ by rhodamine-conjugated phalloidin in the fungusUromyces phaseoli. Eur J Cell Biol 32: 52–58

    PubMed  Google Scholar 

  • Hudspeth AJ (1989) How the ears works work. Nature 341: 397–404

    PubMed  Google Scholar 

  • Jackson SL, Heath IB (1989) Effects of exogenous calcium ions on tip growth, intracellular Ca2+ concentration, and actin arrays in hyphae of the fungusSaprolegnia ferax. Exp Mycol 13: 1–12

    Google Scholar 

  • — — (1990 a) Evidence that actin reinforces the extensible hyphal apex of the oomyceteSaprolegnia ferax. Protoplasma 157: 144–153

    Google Scholar 

  • — — (1990 b) Visualization of actin arrays in growing hyphae of the fungusSaprolegnia ferax. Protoplasma 154: 56–70

    Google Scholar 

  • — — (1992) UV microirradiations elicit Ca2+ dependent apex-directed cytoplasmic contractions in hyphae. Protoplasma 170: 46–52

    Google Scholar 

  • Kropf DL, Berge SK, Quatrano RS (1989) Actin localization duringFucus embryogenesis. Plant Cell 1: 191–200

    PubMed  Google Scholar 

  • Lancelle SA, Hepler PK (1989) Immunogold labeling of actin on sections of freeze-substitued plant cells. Protoplasma 150: 72–74

    Google Scholar 

  • Marks J, Hyams JS (1985) Localization of F-actin through the cell division cycle ofSchizosaccharomyces pombe. Eur J Cell Biol 39: 27–32

    Google Scholar 

  • McKerracher LJ, Heath IB (1986) Polarized cytoplasmic movement and inhibition of saltations induced by calcium-mediated effects of microbeams in fungal hyphae. Cell Motil Cytoskeleton 6: 136–145

    Google Scholar 

  • Mooseker MS (1985) Organization, chemistry and assembly of the cytoskeletal apparatus of the intestinal brush border. Annu Rev Cell Biol 1: 209–241

    PubMed  Google Scholar 

  • Palevitz BA (1987) Accumulation of F-actin during cytokinesis inAllium. Correlation with microtubule distribution and the effects of drugs. Protoplasma 141: 24–32

    Google Scholar 

  • Park D, Robinson PM (1966) Internal pressure of hyphal tips of fungi, and its significance in morphogenesis. Ann Bot NS 119: 425–439

    Google Scholar 

  • Pierson ES, Derksen J, Trass JA (1986) Organization of microfilaments and microtubules in pollen tubes grown in vivo or in vitro in various angiosperms. Eur J Cell Biol 41: 14–18

    Google Scholar 

  • Picton JM, Steer MW (1982) A model for the mechanism of tip extension in pollen tubes. J Theor Biol 98: 15–20

    Google Scholar 

  • — — (1981) Determination of secretory vesicle production rates by dictyosomes in pollen tubes ofTradescantia using cytochalasin D. J Cell Sci 49: 261–272

    PubMed  Google Scholar 

  • Rayle DL, Cleland R (1970) Enhancement of wall loosening and elongation by acid solutions. Plant Physiol 46: 250–253

    Google Scholar 

  • Reinhardt MO (1892) Das Wachstum der Pilzhyphen. Jahrb Wiss Bot 23: 479–565

    Google Scholar 

  • Runeberg P, Raudaskoski M, Virtanen I (1986) Cytoskeletal elements in the hyphae of the homobasidiomyceteSchizophyllum commune visualized with indirect immunofluorescence and NBD-phallacidin. Eur J Cell Biol 41: 25–32

    Google Scholar 

  • Sillers P, Forer A (1981) Autosomal spindle fibres influence subsequent sex-chromosome movements in crane fly spermatocytes. J Cell Sci 49: 51–67

    PubMed  Google Scholar 

  • — — (1983) Action spectrum for changes in spindle fibre birefringence after ultraviolet microbeam irradiations of single chromosomal spindle fibers in crane-fly spermatocytes. J Cell Sci 62: 1–25

    PubMed  Google Scholar 

  • 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 119–141

    Google Scholar 

  • Sampath P, Pollard TD (1991) Effects of cytochalasin, phalloidin, and pH on the elongation of actin filaments. Biochemistry 30: 1973–1980

    PubMed  Google Scholar 

  • Taylor DL, Condeelis JS (1979) Cytoplasmic structure and contractility in amoeboid cells. Int Rev Cytol 56: 57–144

    PubMed  Google Scholar 

  • Uretz RB, Perry RP (1957) Improved ultraviolet microbeam apparatus. Rev Sci Instruments 28: 861–866

    Google Scholar 

  • Wang F, Sampogna RV, Ware BR (1989) pH dependence of actin self-assembly. Biophys J 55: 293–298

    PubMed  Google Scholar 

  • Wessels JGH (1988) A steady-state model for apical wall growth in fungi. Acta Bot Neerl 37: 3–16

    Google Scholar 

  • — (1990) Role of cell wall architecture in fungal tip growth generation. in: Heath IB (ed) Tip growth in plant and fungal cells. Academic Press, San Diego, pp 1–23

    Google Scholar 

  • —, Sietsma JH, Sonnenberg SM (1983) Wall synthesis and assembly during hyphal morphogenesis inSchizophyllum commune. J Gen Microbiol 129: 1607–1616

    Google Scholar 

  • Wilson P, Forer A (1987) Irradiations of rabbit myofibrils with an ultraviolet microbeam. I. Effects of ultraviolet light on the myofibril components necessary for contraction. Biochem Cell Biol 65: 363–375

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Biology Department, York University, 4700 Keele Street, M3J 1P3, North York, Ont., Canada

    Sandra L. Jackson & I. B. Heath

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  1. Sandra L. Jackson
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  2. I. B. Heath
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Jackson, S.L., Heath, I.B. UV microirradiation implicates F-actin in reinforcing growing hyphal tips. Protoplasma 175, 67–74 (1993). https://doi.org/10.1007/BF01403285

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