Vacuolar Lucifer Yellow Uptake in Plants: Endocytosis or Anion Transport; A Critical Opinion
Corresponding Author
D. G. Robinson
Pflanzenphysiologisches Institut, Universität Göttingen, FRG
Pflanzenphysiologisches Institut der Universität Göttingen Untere Karspüle 2 D-3400 Göttingen Federal Republic of GermanySearch for more papers by this authorR. Hedrich
Pflanzenphysiologisches Institut, Universität Göttingen, FRG
Search for more papers by this authorCorresponding Author
D. G. Robinson
Pflanzenphysiologisches Institut, Universität Göttingen, FRG
Pflanzenphysiologisches Institut der Universität Göttingen Untere Karspüle 2 D-3400 Göttingen Federal Republic of GermanySearch for more papers by this authorR. Hedrich
Pflanzenphysiologisches Institut, Universität Göttingen, FRG
Search for more papers by this authorAbstract
Because of its membrane-impermeant-properties Lucifer Yellow-CH (LY) is regarded by animal cell biologists as an ideal tracer for fluid-phase endocytosis. When presented to plant cells or protoplasts this fluoroprobe accumulates in the vacuole. On the other hand there are many cases where LY does not enter the vacuole when loaded into the plant cytosol. These, superficially divergent, results have previously been explained in terms of endocytosis whereby access to the vacuole is considered to occur through vesicle transport. This interpretation has now been challenged in three recent papers where the benzoic acid derivative, probenecid, has been shown to prevent vacuolar LY accumulation in plants. Since probenecid is a well-known inhibitor of organic anion transport in animal cells it has been argued that anion carriers capable of transporting LY might also exist at the plasma membrane and tonoplast of plant cells. Unfortunately probenecid has rarely, if ever, been used in plant transport studies. The fact that it is a weak acid, whose inhibitory effects are observed at concentrations of around 1 mM suggests that caution should prevail when interpreting results obtained with probenecid. The purpose of this article is therefore to highlight the current controversy surrounding LY uptake by plants and to critically evaluate the recent probenecid data.
References
- Barasch, J., Kiss, B., Simon, L., Prince, A., Gruenert, D., Al-Agwati, Q. Defective acidification of intracellular organelles in cystic fibrosis. Nature 352 (1991), 70–73.
- Bianco-Colomas, J., Barthe, P., Orlandini, M., and Le Page-Degivry, T. Carrier-mediated uptake of abscisic acid by suspension cultured Amaranthus tricolor cells. Plant Physiol. 95 (1991), 990–996.
- Boiler, T. and Wiemken, A. Dynamics of vacuolar compartmentation. Ann. Rev. Plant Physiol. 37, (1986), 137–164.
- Brownlee, C., Wood, J. M., and Briton, D. Cytoplasmic free calcium in single cells of centric diatoms. The use of fura-2. Protoplasma 40 (1987), 118–122.
- Bush, D. S. and Jones, R. L. Measurement of cytoplasmic calcium in aleurone protoplasts using indo-1 and fura-2. Cell Calcium (1987), 455–472.
- Bush, D. S. and Jones, R. L. Measuring intracellular Ca2+ levels in plant cells using the fluorescent probes, Indo-1 and Fura-2. Plant Physiol. 93 (1990), 841–845.
- Callaham, D. A. and Hepler, P. K. Detection of calcium fluxes in single plant cells using optical probes (abstract). Calcium research on plants: a workshop on methods, Kona, Hawaii, 1989.
- Clark, K. A. and Goldsmith, M. H. M. Roles of transport and binding in the specific pH-dependent accumulation of auxin by zucchini membrane vesicles. In: Plant Growth Substances (ed. M. Bopp) Springer-Verlag, Berlin (1986), pp. 203–208.
- Clarkson, D. T., Brownlee, C., and Ayling, S. M. Cytoplasmic calcium measurements in intact higher plant cells: results from fluorescence ratio imaging of fura-2. J. Cell Sci. 91 (1988), 71–80.
- Cole, L., Coleman, J., Evans, D., and Hawes, C. Internalization of fluorescein isothiocyante-dextran by suspension-cultured plant cells. J. Cell Sci. 96 (1990), 721–730.
- Cole, L., Coleman, J., Kearnes, A., Morgan, G., and Hawes, C. The organic anion transport inhibitor, probenecid inhibits the transport of Lucifer yellow at the plasma membrane and at the tonoplast in suspension-cultured plant cells. J. Cell Sci 99 (1991), 545–555.
- Cunningham, R. F., Israili, Z. H., and Dayton, P. G. Clinical pharmacokinetics of probenecid. Clinical Pharmacology (NY) 6, (1981), 135–151.
- Deurs, Van B., Peterson, O. W., Olsnes, S., and Sandvig, K. The ways of endocytosis. Int. Rev. Cytol. 17 (1989), 131–177.
- Deus-Neumann, B. and Zenk, M. H. Accumulation of alkaloids in plant vacuoles does not involve an ion-trap mechanism. Planta 167, 44–53.
- Di Virgilio, F., Steinberg, T. H., and Silverstein, S. C. Inhibition of Fura-2 sequestration and secretion with organic anion transport blockers. Call Calcium 11 (1990), 57–62.
- Erwee, M., Goodwin, P., and Van Bel, A. Cell-cell communication in the leaves of Commelina cyanea and other plants. Plant Cell Environ. 8 (1985), 173–178.
- Felle, H. H. Aspects of calcium homeostasis in Riccia fluitans; reactions to perturbations in cytosolic free calcium. Plant Sci. 74 (1991), 27–33.
- Fisher, D. G. Movement of Lucifer Yellow in leaves of Coleus blumei Benth. Plant, Cell, Environ. 11 (1988), 639–644.
- Frachisse, J. M., Johannes, E., and Felle, H. The use of weak acids as physiological tools: a study of the effects of fatty acids on intracellular PH and electrical plasmalemma properties of Riccia fluitans rhizoid cells. Biochem. Biophys. Acta 938 (1988), 199–210.
- Gehring, C. A., Williams, D. A., Cody, S. H., and Parish, R. W. Phototropism and geotropism in maize coleoptiles are spatially correlated with increases in cytosolic free calcium. Nature 345 (1990), 528–529.
- Gerdes, U., Kristensen, J., Moller, J. V., and Sheikh, M. I. Renal handling of phenol red. III. Bidirectional transport. J. Physiol. (Lond.) 277 (1978), 115–129.
- Gilroy, S., Fricker, M. D., Read, N. D., and Trewavas, A. J. Role of calcium in signal transduction of Commelina guard cells. Plant Cell 3 (1991) 333–344.
- Gilroy, S., Hughes, W. A., and Trewavas, A. J. A comparison between Quin-2 and aequorin as indicators of cytoplasmic calcium levels in higher plant cell protoplasts. Plant Physiol 90 (1989), 482–491.
- Gilroy, S., Read, N. D., and Trewavas, A. J. Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate imitates stomatal closure. Nature 346 (1990), 769–771.
- Goodwin, P. B., Shepherd, V., and Erwee, M. G. Compartmentation of fluorescent tracers injected into the epidermal cells of Egeria densa leaves. Planta 181 (1990), 129–136.
-
Guern, J.,
Renaudin, J. P., and
Brown, S. C.
The compartmentation of secondary metabolites in plant cell cultures. In: Cell culture and somatic cell genetics (ed.
F. Constabel &
I. K. Vasil), Academic Press, New York (1987), pp. 43–76.
10.1016/B978-0-12-715004-8.50009-0 Google Scholar
- Hedrich, R. and Kurkdjian, A. Characterization of an anion-permeable channel from sugar beet vacuoles: effect of inhibitors. EMBO Journ. 7 (1988), 3661–3666.
- Hedrich, R. and Schroeder, J. 1. The physiology of ion channels and electrogenic pumps in higher plants. Ann. Rev. Plant Physiol. Mol. Biol. 40 (1989), 539–569.
- Hepler, P. K.–Cited in: Bioprobes Nr. 13, (1991).
- Herzog, V. and Reggio, H. Pathways of endocytosis from luminal plasma membrane in rat exocrine pancreas. European Journal of Cell Biology 21 (1980), 141–150.
- Heuser, J. E. Effects of cytoplasmic acidification on clathrin lattice morphology. J. Cell Biol. 108 (1989), 401–411.
- Hilmer, S., Hedrich, R., Robert-Nicoud, M., and Robinson, D. G. Uptake of Lucifer yellow CH in leaves of Commelina communis is mediated by endocytosis. Protoplasma 158 (1990), 142–148.
- Hillmer, S., Quader, H., Robert-Nicoud, M., and Robinson, D. G. Lucifer yellow uptake in cells and protoplasts of Daucus carota visualized by laser scanning microscopy. J. Exp. Bot. 40 (1989), 417–423.
- Kaiser, W. M. and Hartung, W. Uptake and release of abscisic acid by isolated photoautotrophic mesophyll cells, depending on pH gradients. Plant Physiol. 68 (1981), 202–206.
- Kamen, B. A., Wang, M.-T., Streckfuss, A. J., Peryea, X., and Anderson, R. G. W. Delivery of folates to the cytoplasm of MA104 cells is mediated by a surface membrane receptor that recycles. J. Biol. Chem. 25 (1988), 13602–13609.
- Kamen, B. A., Smith, A. K., and Anderson, R. G. W. The folate receptors works in tandem with a probenecid-sensitive carrier in MA104 cells in vitro. J. Clin. Invest. 87 (1991), 1442–1449.
- Keller, B. U., Hedrich, R., and Raschke, K. Voltage-dependent anion channels in the plasma membrane of guard cells. Nature 341 (1989), 450–452.
- Kreis, W. and Reinhard, E. Selective uptake and vacuolar storage of primary cardiac glycosides by suspension-cultured Digitalis lanata cells. J. Plant Physiol. 128 (1987), 311–326.
- Kurkdjian, A. and Guern, J. Intracellular pH: measurement and importance in cell activity. Ann. Rev. Plant Physiol. Plant Mol. Biol. 40 (1989), 271–303.
- Lipman, B. J., Silverstein, S. C., and Steinberg, T. H. Organic anion transport in macrophage membrane vesicles. J. Biol. Chem. 265 (1990), 2142–2147.
- Lowy, R. J. and Spring, K. R. Identification of riboflavin transport by MDCK cells using quantitative fluorescence video microscopy. J. Membrane Biol. 117 (1990), 91–99.
- Madore, M. A., Oross, J. W. and Lucas, W. J. Symplastic transport in Ipomea tricolor source leaves. Plant Physiol. 82 (1986), 432–442.
- Marin, B. Plant Vacuoles. Their importance in solute compartmentation in cells and their applications in plant biotechnology. pp. 1–562.NATO AS1 Series. Plenum press. New York (1987).
- Marten, S., Busch, H., Raschke, K., and Hedrich, R. Modulation of voltage-dependent gating of the plasma membrane anion channel in guard cells. EMBO Journ. (1991) (submitted).
- Matern, U., Reichenbach, C., and Heller, W. Efficient uptake of flavonoids into parsley (Petroselinum hortense) vacuoles requires acylated glycosides. Planta 167 (1986), 183–189.
- Matile, P. Das toxische Kompartiment der Pflanzenzelle. Naturwiss. 71 (1984), 18–24.
- McAinsh, M. R., Brownlee, C., and Hetherington, A. M. Abscisic acid-induced elevation of guard cell cytosolic Ca2+ precedes stomatal closure. Nature 343 (1990), 186–188.
- Mellman, I., Fuchs, R., and Helenius, A. Acidification of the endocytic and exocytic pathways. Ann. Rev. Biochem. 55 (1986), 663–700.
- Mende, P. and Wink, M. Uptake of the quinolizidine alkaloid lupanine by protoplasts and vacuoles of Lupinus polyphyllus cell suspension cultures. Diffusion or carrier-mediated transport J. Plant Physiol. 129 (1987), 229–242.
- Miller, D., Callahan, D., Gross, D., and Hepler, P. K. Free Ca2+ gradients in pollen tubes. Nature (1991) (submitted).
- Møller, J. V. and Sheikh, Igbal M. Renal organic anion transport system: pharmacological, physiological and biochemical aspects. Pharmacol. Reviews vol. 34 (1983), No. 4315–359.
- Murer, H. and Burckhardt, G. Membrane transport of anions across epithelia of mammalian small intestine and kidney proximal tubule. Rev. Physiol. Biochem. Pharmacol. 96 (1983), 1–51.
- Nobiling, R. and Reiss, H.-D. Quantitative analysis of calcium gradients and activity in growing pollen tubes of Lilium longiflorum Protoplasma 39 (1987), 20–24.
- Nour, J. M. and Rubery, P. H. The uptake of gibberellin A, by suspension-cultured Spinacia oleracea cells has a carrier-mediated component. Planta 160 (1984), 436–443.
- O'Driscoll, D., Wilson, G., and Steer, M. W. Lucifer yellow and fluorescein isothiocyanate uptake by cells of Morinda citrifolia in suspension cultures is not confined to the endocytic pathway. J. Cell Sci (1991) (in press).
- Oparka, K. J., Murant, E. A., Wright, K. M., Prior, D. A. M., and Harris, N. The drug probenecid inhibits the vacuolar accumulation of fluorescent anions in onion epidermal cells. J. Cell Science 99 (1991), 557–563.
- Oparka, K. J. Uptake and compartmentation of fluorescent probes by plant cells. Journal of Experimental Botany, 42 (1991), 565–579.
- Oparka, K. J., Robinson, D. G., Prior, D. A. M., Derrick, P., and Wright, K. Uptake of lucifer yellow CH into intact barley roots: Evidence for fluid phase endocytosis. Planta 176 (1988), 541–547.
- Owen, T. P., Platt-Aloia, K. A., and Thomson, W. W. Ultrastructural localization of Lucifer yellow and endocytosis in plant cells. Protoplasma 60 (1991), 115–120.
- Palevitz, B. A. and Hepler, P. K. Changes in dye coupling of stomatal cells of Allium and Commelina demonstrated by microinjection of Lucifer Yellow. Planta 164 (1985), 473–479.
- Pistocchi, R., Keller, F., Bagni, N., and Matile, P. Transport and subcellular localization of polyamines in carrot protoplasts and vacuoles. Plant Physiol. 7 (1988), 514–518.
- Quader, H. and Fast, H. Influence of cytosolic pH changes on the organisation of the endoplasmic reticulum in epidermal cells of onion bulb scales: acidification by loading with weak organic acids. Protoplasma 157 (1990), 216–224.
- Ranjeva, R., Carrasco, A., and Boudet, A. M. Inositol triphosphate stimulates the release of calcium from intact vacuoles isolated from Acer cells. FEBS Lett. 230 (1988), 137–141.
- M. F. Roberts Papaver latex and alkaloid storage vacuoles. In: Plant vacuoles. Their importance in solute compartmentation in cells and their application in plant biotechnology. (ed. B. Marin) pp. 513–528.NATO Advanced Institute Series 134, (1987).
- Robinson, D. G. and Hillmer, S. Endocytosis in plants. Physiologia Plantarum 79 (1990), 96–104.
- Robinson, D. G., Hedrich, R., Herkt, B., Diekmann, W., and Robert-Nicoud, M. Endocytosis in plants: problems and perspectives. In: Proceedings of the second european workshop on endocytosis. ( P. Courtoy, J. Gruenberg, L. Mata, M. Marsh, B. Deurs eds.) NATO/ASI Series. Springer Verlag (1991), (in press).
-
Robinson, D. G.
“Piggy-Back” Endocytosis: vitamin-mediated uptake of macromolecules into plant cells.
Botanica Acta
103 (1991), 85–86.
10.1111/j.1438-8677.1991.tb00200.x Google Scholar
- Rothberg, K. G., Ying, Y., Kolhouse, J. F., Kamen, B. A., and Anderson, R. G. W. The glycophospholipid-like folate receptor internalizes folate without entering the clathrin-coated pit endocytic pathway. J. Cell. Biol. 110 (1990), 637–649.
- Russ, U., Grolig, F., and Wagner, G. Changes of cytoplasmic free Ca2+ in the green alga Mougeotia scalaris as monitored with indo-1, and their effect on the velocity of chloroplast movements. Planta 184 (1991), 105–112.
- Sandvig, K., Olsnes, S., Petersen, O. W., and Van Deurs, B. Acidification of the cytosol inhibits endocytosis from coated pits. J. Cell Biol. 105 (1987), 679–689.
- Schroeder, J.I. and Hagiwara, S. Repetitive increases in cytosolic Ca2+ of guard cells by abscisic acid activation of nonselective Ca2+ permeable channels. Proc. Nat. Acad. Sci (USA) 87 (1990), 9305–9309.
- Steinberg, T. H., Swanson, J. A., and Silverstein, S. C. Aprelysosomal compartment sequesters membrane-impermeant fluorescent dyes from the cytoplasmic matrix of J774 macrophages. J. Cell Biol. 107 (1988), 887–896.
- Steinberg, T. H., Newman, A. S., Swanson, J. A., and Silverstein, S. C. Macrophages possess probenecid-inhibitable organic anion transporters that remove fluorescent dyes from the cytoplasmic matrix. J. Cell Biol. 105 (1987), 2695–2702.
- Steinberg, T. H., Newman, A. S., Swanson, J. A., and Silverstein, S. C. ATP4– permeabilizes the plasma membrane of mouse macrophages to fluorescent dyes. J. Biol. Chem. 262 (1987), 8884–8888.
- Steinbiss, H. and Sabel, P. Protoplasts derived from tobacco cells can survive capillary microinjection of the fluorescent dye Lucifer yellow. Protoplasma 116 (1983), 223–227.
- Stewart, W. W. Lucifer dyes — highly fluorescent dyes for biological tracing. Nature 292 (1981), 17–21.
- Taghert, P. H., Bastiani, M. J., Ho, R. K., and Goodman, C. S. Guidance of pioneer growth cones: filopodial contacts and coupling revealed with an antibody to Lucifer Yellow. Dev. Biology 94 (1982), 391–399.
- Terry, B. R. and Robards, A. W. Hydrodynamic radius alone governs the mobility of molecules through plasmodesmata. Planta 171 (1987), 145–157.
- Tucker, J. E., Mauzerall, D., and Tucker, E. B. Symplastic transport of carboxyfluorescein in stained hairs of Setcreasea purpureais is diffusive and includes loss to the vacuole. Plant Physiol. 90 (1989), 1143–1147.
- Turgeon, R. and Hepler, P. K. Symplastic continuity between mesophyll and companion cells in minor veins of mature Cucurbita pepo L. leaves. Planta 179 (1989), 24–31.
- Wangemann, P., Wittner, M., Di Stefano, A., Englert, H. C., Lang, H. C., Schlatter, E., and Greger, R. Cl−-channel blockers in the thick ascending limb of the loop of Henle Structure activity relationship. Pflügers Arch. 407 (1986), (Suppl. 2), 128–141.
- Werner, C. and Matile, P. Accumulation of coumaryl glycosides in vacuoles of barley mesophyll protoplasts. J. Plant Physiol. 118 (1985), 237–249.
- Wink, M. Physiology of secondary product formation in plants. In: Secondary products from plant tissue culture (ed. B. V. Charlwood, and M. J. C. Rhodes). Proc. Phytochem. Soc. Eur. pp. 23–41.Clarendon Press, Oxford (1990).
- Wright, K. M. and Oparka, K. J. Uptake of Lucifer Yellow CH into plant-cell protoplasts: a quantitative assessment of fluid-phase endocytosis. Planta 179 (1989), 257–264.