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Actin and the elongation of plant cells

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Summary

We have investigated in parallel the effects of different types of inhibitors on elongation of oat coleoptile cells in IAA and on the integrity of the longitudinally oriented actin-containing microfilaments present in control cells as detected by rhodamine phalloidin (RP) staining. Where growth was 50% inhibited by cytochalasin D (CD), we observed extensive to complete breakdown of the microfilaments (MFs) with the appearance of new RP staining in a few nuclei and markedly along the cross walls. When the CD-treated coleoptiles were held at 4°C the nuclei were uniformly strongly stained and cross wall staining was not seen, suggesting that translocation to the nuclei may be an intermediate step in final disposition of the actin. The divalent ions calcium and magnesium both inhibited growth in a dose dependent way, with calcium giving 50% inhibition at 65 mM and magnesium at 25 mM. KCl was not inhibitory and did not reverse the inhibition by divalent ions even at 250 mM. At 50% inhibition by either ion, the long MFs in many cells were replaced either by short fragmented MFs and small brightly staining granules (calcium) or by short usually twisted MFs and large, less intensely staining masses (magnesium). Iodoacetate at 2mM inhibited growth almost completely and resulted in short, fragmented, twisted or curled MFs in most of the cells. Abscisic acid also caused replacement of some MFs with faintly fluorescent bodies somewhat larger than those in CaCl2; occasionally granules similar to those in CaCl2 were also seen. Only mannitol and galactose, which inhibit growth by their osmotic effect, did not cause breakup of the MFs; indeed the MFs in mannitol appeared if anything wider and thicker. The results show that under the influence of three types of growth inhibitors the actin-containing MFs in the cells are broken down to different extents resulting in new structures. The results support the idea that the integrity of the MF bundles is linked, perhaps causally, to the elongation of theAvena cells.

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Abbreviations

IAA:

indoleacetic acid

ABA:

abscisic acid

CD:

cytochalasin D

MF:

microfilaments

MFB:

microfilament bundles

RP:

rhodamine phalloidin

References

  • Brett JG, Godman GC (1986) Cytoskeletal organization affects cellular responses to cytochalasins: comparison of a normal line and its transformants. Tissue Cell 18: 175–199

    PubMed  Google Scholar 

  • Cande WZ, Goldsmith MHM, Ray PM (1973) Polar auxin transport and auxin-induced elongation in the absence of cytoplasmic streaming. Planta 111: 279–296

    Google Scholar 

  • Carlier MF (1991) Actin: protein structure and filament dynamics. J Biol Chem 266: 1–4

    PubMed  Google Scholar 

  • Cooper JS (1991) The role of actin polymerization in cell motility. Annu Rev Physiol 53: 585–605

    PubMed  Google Scholar 

  • Cosgrove DJ (1987) Better understanding of plant growth is likely to come from in-depth studies of the characteristics and mechanisms of wall relaxation. In: Cosgrove DJ, Knievel DP (eds) Physiology of cell expansion during plant growth. American Society of Plant Physiologists, Rockville, MD, pp 88–104

    Google Scholar 

  • Devrietos PN, Zigmond S (1988) Chemotaxis in energetic cells; a focus on leucocytes andDictyostelium. Annu Rev Cell Biol 84: 649–696

    Google Scholar 

  • Forscher P, Smith SJ (1988) Actions of cytochalasins on the organizations of actin filaments and microtubules in a neuronal growth cone. J Cell Biol 107: 1502–1516

    Google Scholar 

  • Hall AL, Schlein A, Condeelis J (1988) Relationship of pseudopod extension to chemotactic hormone induced actin polymerization in amoeboid cells. J Cell Biochem 37: 285–299

    PubMed  Google Scholar 

  • Hedberg KK, Birrel GB, Habliston DL, Griffith OH (1991) Staurosporin induces dissolution of microfilament bundles by a protein kinase C independent pathway. Exp Cell Res 188: 199–208

    Google Scholar 

  • Hayashi T (1989) Xyloglucans in the primary cell wall. Annu Rev Plant Physiol 40: 139–168

    Google Scholar 

  • Heslop-Harrison J, Heslop-Harrison Y (1991) Restoration of movement and apical growth in the angiosperm pollen tube following cytochalasin-induced paralysis. Philos Trans R Soc Lond [Biol] 331: 225–235

    Google Scholar 

  • Johnson P (1990) Calpains (intracellular calcium-activated cysteine proteinases): structure-activity relationships and involvement in normal and abnormal cellular metabolism. Int J Biochem 22: 811–822

    PubMed  Google Scholar 

  • Kaufman D, Thimann KV (1958) Cytoplasmic streaming in the cambium of white pine. In: Thimann KV (ed) The physiology of forest trees. Ronald Press, New York, pp 479–492

    Google Scholar 

  • Kelso JM, Turner JS (1955) Protoplasmic streaming inTradescantia. I. The effects of IAA and other growth-promoting substances on streaming. Aust J Biol Sci 8: 11–35

    Google Scholar 

  • Kersey YM, Hepler PK, Palevitz BA, Wessells NK (1976) Polarity of actin filaments in characean algae. Proc Natl Acad Sci USA 73: 165–167

    PubMed  Google Scholar 

  • Kohno T, Shimmen R (1987) Ca2+-induced fragmentation of actin filaments in pollen tubes. Protoplasma 141: 177–179

    Google Scholar 

  • Kutschera U, Scopfer P (1986) Effects of auxin and abscisic acid on cell wall extensibility in maize coleoptiles. Planta 167: 527–535

    Google Scholar 

  • Labavitch JM, Ray PPM (1974) Relationship between promotion of xyloglucan metabolism and initiation of elongation by IAA. Plant Physiol 54: 497–502

    Google Scholar 

  • Matsudaira P, Janmey P (1988) Pieces in the actin-severing protein puzzle. Cell 54: 139–140

    PubMed  Google Scholar 

  • McLean B, Shurong H, McKinney ES, Meagher RB (1990) Plants contain highly divergent actin variants. Cell Motil Cytoskeleton 17: 374–390

    Google Scholar 

  • Meagher RB, McClean BG (1990) Diversity of plant actin. Cell Motil Cytoskeleton 16: 164–166

    Google Scholar 

  • Nagai R, Hayama T (1979) Ultrastructural aspects of cytoplasmic streaming in characean cells. In: Hatano S, Ishikawa H, Sato H (ed) Cell motility, molecules and organization. University of Toronto Press, Toronto, pp 321–337

    Google Scholar 

  • O'Brien TP, Thimann KV (1966) Intracellular fibers in oat coleoptile cells and their possible significance in cytoplasmic streaming. Proc Natl Acad Sci USA 56: 888–894

    PubMed  Google Scholar 

  • Palevitz BA (1980) Comparative effects of phalloidin and cytochalasin B on motility and morphogenesis inAllium. Canad J Bot 58: 773–785

    Google Scholar 

  • Palevitz BA (1988) Cytochalasin-induced reorganization inAllium root cells. Cell Motil Cytoskeleton 9: 283–298

    Google Scholar 

  • —, Ash JF, Hepler PK (1974) Actin in the green alga,Nitella. Proc Natl Acad Sci USA 71: 363–366

    PubMed  Google Scholar 

  • Parthasarathy MV (1985) F-actin architecture in coleoptile epidermal cells. Eur J Cell Biol 39: 1–12

    Google Scholar 

  • —, Pardue TD, Witztum A, Alvernaz JA (1988) Actin network a normal component of the cytoskeleton in many vascular plant cells. Amer J Bot 72: 1318–1323

    Google Scholar 

  • Pope DG, Thorpe JR, Al-Azzxawi MJ, Hall JL (1979) The effect of cytochalasin B on the rate of growth and ultrastructure in wheat coeoptiles and maize roots. Planta 144: 373–383

    Google Scholar 

  • Ray PJ (1973) Regulation of β-glucan synthetase activity by auxin in pea stem tissue I. Kinetic aspects. II. Metabolic requirements. Plant Physiol 51: 601–608, 609–614

    Google Scholar 

  • Sanger JW, Gwinn J, Sanger JM (1980) Dissolution of cytoplasmic actin bundles and the induction of nuclear bundles by dimethyl sulfoxide. J Exp Zool 213: B 227–230

    PubMed  Google Scholar 

  • Sweeney BM, Thimann KV (1937) The effect of auxins on protoplasmic streaming. I. J Gen Physiol 21: 123–135

    Google Scholar 

  • — — (1938) The effect of auxins on protoplasmic streaming. II. J Gen Physiol 21: 439–461

    Google Scholar 

  • Theriot JA, Mitchison TJ (1991) Actin microfilament dynamics in locomoting cells. Nature 352: 126–131

    PubMed  Google Scholar 

  • Tchakarov L, Vitale M-L, Jeyepragasan M, Rodriguez del Castillo A, Trifaro J-M (1990) Expression of scinderin, an actin filament-severing protein, in different tissues. FEBS Lett 268: 209–212

    PubMed  Google Scholar 

  • Thimann KV, Bonner WD (1948) Experiments on the growth and inhibition of isolated plant parts. I. The action of iodoacetate and organic acids on theAvena coleoptile. Amer J Bot 25: 271–281

    Google Scholar 

  • —, Schneider CL (1938) The role of salts, hydrogen-ion concentration and agar in the response ofAvenacoleoptiles to auxin. Amer J Bot 25: 270–280

    Google Scholar 

  • Tilney LC, Hatano S, Ishikawa H, Mooseker MS (1973) The polymerization of actin; its role in the generation of the acrosomal process of certain echinoderm sperm. J Cell Biol 59: 109–126

    PubMed  Google Scholar 

  • Urbanik E, Ware BR (1989) Actin filament capping and cleaving activity of cytochalasins B, D, E, and H. Arch Biochem Biophys 269: 181–187

    PubMed  Google Scholar 

  • Wakabayashi K, Sujurai N, Kuraishi S (1989) Role of the outer tissue in abscisic acid-mediated growth suppression of etiolated squash hypocotyl segments. Physiol Plant 75: 151–156

    Google Scholar 

  • Warrick HW, Spudich JA (1987) Myosin structure and function in cell motility. Annu Rev Cell Biol 3: 379–421

    PubMed  Google Scholar 

  • Wayne R, Staves MP, Leopold AC (1992) The contribution of the extracellular matrix to gravisensing in characean cells. J Cell Sci 101: 611–623

    PubMed  Google Scholar 

  • Zeevardt JAD, Creelman RR (1988) Metabolism and physiology of abscisic acid. Annu Rev Plant Physiol 39: 439–472

    Google Scholar 

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  1. Department of Cell and Developmental Biology, The School of Medicine, University of Pennsylvania, 19104-6058, Philadelphia, PA, USA

    K. V. Thimann, K. Reese & V. T. Nachmias

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  1. K. V. Thimann
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  2. K. Reese
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  3. V. T. Nachmias
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Thimann, K.V., Reese, K. & Nachmias, V.T. Actin and the elongation of plant cells. Protoplasma 171, 153–166 (1992). https://doi.org/10.1007/BF01403730

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