Abstract
The magnitude and spatial localization of Ca2+, K+ and H+ fluxes in growing and non-growing Limnobium stoloniferum root hairs was determined using non-invasive, ion-selective vibrating microelectrodes. Both the spatial pattern and magnitude of the ionic flux was dependent on the particular ion in question. Both H+ and Ca2+ influx was localized almost exclusively to the tips of growing root hairs, suggesting that these fluxes may be involved in directing growth. Influx of K+ showed no distinct localization and uptake appeared uniform along the length of the root hair. Competitive inhibition of Ca2+ influx using a range of Mg+ concentrations indicated that the magnitude of the Ca2+ flux entering the root hair tip did not determine growth rate; however, the presence of Ca2+ on the external face of the membrane was implicit for root hair integrity. Aluminum proved to be a potent inhibitor of root hair growth. At an exogenous Al concentration of 20 μM a complete blockage of Ca2+ influx into root hair tips was observed, suggesting that Al blockage of Ca2+ influx could be involved in Al toxicity. However, at a lower Al concentration (2 μM), Ca2+ fluxes were unaffected while inhibition of growth was still observed along with a distinct swelling of the root hair tip. The swelling at the root hair tips was identical in appearance to that seen in the presence of microtubule inhibitors, suggesting that Al could influence a number of different sites at the plasma-membrane surface and within the cell. The possible role(s) of Ca2+ and H+ fluxes in directing tip growth are discussed.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Anghileri LJ (1992) Ehrlich tumour cells: Ca2+-uptake modification by aluminium lactate. Cell Calcium 13: 277–279
Barley KP, Rovira AD (1970) The influence of root hairs on the uptake of phosphate. Soil Sci Plant Anal 1: 287–292
Biffen M, Hanke DE (1990) Polyphosphoinositidase activity in soybean membranes is Ca2+ dependent and shows no requirement for guanine-nucleotides. Plant Sci 69: 147–155
Combettes L, Champeil P (1994) Calcium and inositol 1,4,5-triphosphate-induced Ca2+ release. Science 265: 813
Creutz CE (1992) The annexins and exocytosis. Science 258: 924–931
Deleers M, Servais JP, Wülfert E (1986) Neurotoxic cations induce membrane rigidification and membrane fusion at micromolar concentrations. Biochim Biophys Acta 855: 271–276
Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.).II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol 103: 695–702
Emons AM (1987) The cytoskeleton and secretory vesicles in root hairs of Equisetum and Limnobium and cytoplasmic streaming in root hairs of Equisetum. Ann Bot 60: 625–632
Felle H (1988) Cytoplasmic free calcium in Riccia fluitans L. and Zea mays L.: Interaction of Ca2+ and pH? Planta 176: 248–255
Foy CD, Chaney RL, White MC (1978) The physiology of metal toxicity in plants. Annu Rev Plant Physiol 29: 511–566
Fray JCS, Park CS, Valentine AND (1987) Calcium and the control of renin secretion. Endocrinol Rev 8: 53–93
Gassman W, Schroeder JI (1994) Inward-rectifying K+ channels in root hairs of wheat: A mechanism for aluminum-sensitive low-affinity K+ uptake and membrane potential control. Plant Physiol 105: 1399–1408
Gibbon BC, Kropf DL (1994) Cytosolic pH gradients associated with tip growth. Science 263: 1419–1421
Gomperts BD (1990) GE: a GTP-binding protein mediating exocytosis. Annu Rev Physiol 52: 591–606
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, Orlando, Fla, pp 59–90
Heath IB (1990) Tip growth in plant and fungal cells. Academic Press, Orlando, Fla
Huang JW, Shaff JE, Grunes DL, Kochian LV (1992) Aluminum effects on calcium fluxes at the root apex of aluminum-tolerant and aluminum-sensitive wheat cultivars. Plant Physiol 98: 230–237
Huang JW, Grunes DL, Kochian LV (1994) Voltage-dependent Ca2+ influx into right-side-out plasma membrane vesicles isolated from wheat roots: Characterization of a putative Ca2+ channel. Proc Natl Acad Sci USA 91: 3473–3477
Kerboeuf D, Cohen J (1990) A Ca2+ influx associated with exocytosis is specifically abolished in a Paramecium exocytotic mutant. J Cell Biol 111:2527–2535
Kiehart DP (1981) Studies on the in vivo sensitivity of spindle microtubles to calcium ions and evidence for a vesicular calcium-sequestering system. J Cell Biol 88: 604–617
Knoll G, Grässle A, Braun C, Probst W, Höhne-Zell B, Plattner H (1993) A calcium influx is neither strictly associated with nor necessary for exocytotic membrane fusion in Paramecium cells. Cell Calcium 14: 173–185
Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46: 237–260
Kochian LV, Shaff JE, Kühtreiber WM, Jaffe LF, Lucas WJ (1992) Use of an extracellular ion-selective, vibrating microelectrode system for the quantification of K+, H+, and Ca2+ fluxes in maize roots and maize suspension cells. Planta 188: 601–610
Kühtreiber WM, Jaffe LF (1990) Detection of extracellular calcium gradients with a calcium-specific vibrating electrode. J Cell Biol 110: 1563–1573
Lazof DB, Goldsmith JG, Rufty TW, Linton RW (1994) Rapid uptake of aluminum into cells of intact soybean root tips: A microanalytical study using secondary ion mass spectrometry. Plant Physiol 106: 1107–1114
Miller AL, Gow NAR (1989) Correlation between profile of ion-current circulation and root development. Physiol Plant 75: 102–108
Miller DD, Callaham DA, Gross DJ, Hepler PK (1992) Free Ca2+ gradient in growing pollen tubes of Lilium. J Cell Sci 101: 7–12
Nuccitelli R (1983) Transcellular ion currents: Signals and effectors of polarity. Mod Cell Biol 2: 451–481
Parker DR, Chaney RL, Norvell WA (1995) GEOCHEM-PC: A chemical speciation program for IBM and compatible computers. In: Loeppert RH (ed) Chemical equilibria and reaction models. Soil Science Society of America, Madison, Wis, pp 253–270
Pellet DM, Grunes DL, Kochian LV (1995) Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196: 788–795
Picton JM, Steer MW (1983) Evidence for the role of Ca2+ ions in tip extension in pollen tubes. Protoplasma 115: 11–17
Pierson ES, Miller DD, Callaham DA, Shipley AM, Rivers BA, Cresti M, Hepler PK (1994) Pollen tube growth is coupled to extracellular calcium gradient: Effect of BAPTA-type buffers and hypertonic media. Plant Cell 6: 1815–1828
Plattner H, Stürzl R, Matt H (1985) Synchronous exocytosis in Paramecium cells.IV. Polyamino compounds as potent trigger agents for repeatable trigger-redocking sites. Eur J Cell Biol 36: 32–37
Przybylski RJ, Szigeti V, Davidheiser S, Kirby AC (1994) Calcium regulation of skeletal myogenesis.II. Extracellular and cell surface effects. Cell Calcium 15: 132–142
Ryan PR, Kochian LV (1993) Interaction between aluminum toxicity and calcium uptake at the root apex in near-isogenic lines of wheat (Triticum aestivum L.) differing in aluminum tolerance. Plant Physiol 102: 975–982
Ryan PR, Di Tomaso JM, Kochian LV (1993) Aluminum toxicity in roots: An investigation of spatial sensitivity and the role of the root cap. J Exp Bot 44: 437–446
Schiefelbein JW, Shipley A, Rowse P (1992) Calcium influx at the tip of growing root-hair cells of Arabidopsis thaliana. Planta 187: 455–459
Shi B, Chou K, Haug A (1993) Aluminum impacts elements of the phosphoinositol signalling pathway in neuroblastoma cells. Mol Cell Biochem 121: 109–118
Smith JS, Sanger RH, Jaffe LF (1994) The vibrating Ca2+ electrode: A new technique for detecting plasma membrane regions of Ca2+ influx and efflux. Methods Cell Biol 40: 115–134
Steer MW (1988) The role of calcium in exocytosis and endocytosis in plant cells. Physiol Plant 72: 213–220
Steer MW, Steer JM (1989) Pollen tube tip growth. New Phytol 111: 323–358
Taylor AR, Brownlee C (1992) Localised patch clamping of plasma membrane of a polarized plant cell: Laser microsurgery of the Fucus spiralis rhizoid cell wall. Plant Physiol 99: 1686–1688
Van Ginkel MF, Van der Voet GB, Van Eijk HG, Wolff FA (1990) Aluminum binding to serum constituents: A role for transferrin and for citrate. J Clin Chem Clin Biochem 28: 459–464
Vierstra R, Haug A (1978) The effects of Al3+ on the physical properties of membrane lipids in Thermoplasma acidophilum. Biochem Biophys Res Commun 84: 138–143
White JM (1992) Membrane fusion. Science 258: 917–924
Wollheim CB, Lang J (1994) A game plan for exocytosis. Trend Cell Biol 4: 339–341
You G, Nelson DJ (1991) Aluminum ion vs. calcium ion binding to methionine and tyrosine spin-labelled bovine brain calmodulin. J Inorg Biochem 41: 283–292
Zorec R, Tester M (1992) Cytoplasmic calcium stimulates exocytosis in a plant secretory cell. Biophys J 63: 864–867
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Jones, D.L., Shaff, J.E. & Kochian, L.V. Role of calcium and other ions in directing root hair tip growth in Limnobium stoloniferum . Planta 197, 672–680 (1995). https://doi.org/10.1007/BF00191575
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00191575