Summary
Two free-space marker procedures (Prussian blue and lanthanum nitrate) were employed to determine the pathway(s) followed by water and solutes in the transpiration stream after their introduction into the xylem of small and intermediate bundles, and the effectiveness of the suberin lamellae of the bundle-sheath cells as a barrier to the movement of tracer ions (Fe3+ and La3+). Judged from the distribution of Prussian-blue crystals (insoluble, crystalline deposits resulting from the precipitation of ferric ions by ferrocyanide anions) and lanthanum deposits, water and the tracer ions moved readily from the lumina of the vessels into the apoplast (cell wall continuum) of the phloem and bundle-sheath cells via portions of vessel primary walls not bearing lignified secondary wall thickenings. Prussian blue and lanthanum deposits were abundant on the bundlesheath cell side of the bundle sheath/mesophyll interface but few occurred on that of the mesophyll, indicating that the suberin lamella is an effective barrier to apoplastic movement of both ferric and lanthanum ions. The presence of Prussian-blue crystals and lanthanum deposits in the compound middle lamella of the radial wall of the bundle-sheath cells indicates that the compound middle lamella provides an apoplastic pathway for transpirational water from the xylem to the evaporating surfaces of the mesophyll and epidermal cells.
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References
Bannister, L. H., 1971: Lanthanum as an intracellular stain. J. Microscopy95, 413–419.
Botha, C. E. J., Evert, R. F., Cross, R. H. M., Marshall, D. M., 1982: The suberin lamella, a possible barrier to water movement from the veins to the mesophyll ofThemeda triandra Forsk. Protoplasma112, 1–8.
Byott, G. S., Sheriff, D. W., 1976: Water movement into and throughTradescantia virginiana (L.) leaves. II. Liquid flow pathways and evaporative sites. J. exp. Bot.27, 634–639.
Campbell, N., Thomson, W. W., Platt, K., 1974: The apoplastic pathway of transport to salt glands. J. exp. Bot.25, 61–69.
Crowdy, S. H., Tanton, T. W., 1970: Water pathways in higher plants. I. Free space in wheat leaves. J. exp. Bot.21, 102–111.
DuPont, F. M., Leonard, R. T., 1977: The use of lanthanum to study the functional development of the Casparian strip in corn roots. Protoplasma91, 315–323.
Eleftheriou, E. P., Tsekos, I., 1979: Development of mestome sheath cells in leaves ofAegilops comosa var.thessalica. Protoplasma100, 139–153.
Eschrich, W., 1975: Sealing systems in phloem. In: Encycl. plant physiol. Vol. 1. Transport in Plants I (Zimmermann, M. H., Milburn, J. A., eds.), pp. 39–56. Berlin-Heidelberg-New York: Springer.
Esau, K., 1977: Anatomy of seed plants, 2nd ed. New York: J. Wiley and Sons.
Espelie, K. E., Kolattukudy, P. E., 1979: Composition of the aliphatic components of “suberin” from the bundle sheaths ofZea mays leaves. Plant Sci. Lett.15, 225–230.
Evert, R. F., 1980: Vascular anatomy of angiospermous leaves, with special consideration of the maize leaf. Ber. dtsch. bot. Ges.93, 43–55.
—, 1982: Sieve-tube structure in relation to function. BioScience32, 789–795.
—,Eschrich, W., Heyser, W., 1977: Distribution and structure of the plasmodesmata in mesophyll and bundle-sheath cells ofZea mays L. Planta136, 77–89.
—, 1978: Leaf structure in relation to solute transport and phloem loading inZea mays L. Planta138, 279–294.
Fahimi, H. D., Cotran, R. S., 1971: Permeability studies in heatinduced injury of skeletal muscle using lanthanum as fine structural tracer. Amer. J. Path.62, 142–157.
Fineran, B. A., Gilbertson, J. M., 1980: Application of lanthanum and uranyl salts as tracers to demonstrate apoplastic pathways for transport in glands of the carnivorous plantUtricularia monanthos. Euro. J. Cell Biol.23, 66–72.
Fritz, E., Evert, R. F., Heyser, W., 1983: Microautoradiographic studies of phloem loading and transport in the leaf ofZea mays L. Planta159, 193–206.
Gunning, B. E. S., Pate, J. S., 1969: “Transfer cell.” Plant cells with wall ingrowths, specialized in relation to short distance transport of solutes—Their occurrences, structure, and development. Protoplasma68, 107–133.
Hanzely, L., Harmet, K. H., 1982: Effect of lanthanum on cell wall elongation inAvena coleoptile segments: physiological and ultrastructural studies. Z. Pflanzenphysiol.107, 223–230.
Hattersley, P. W., Browning, A. J., 1981: Occurrence of the suberized lamella in leaves of grasses of different photosynthetic types. I. In parenchymatous bundle sheaths and PCR (“Kranz”) sheaths. Protoplasma109, 371–401.
Heyser, W., Evert, R. F., Fritz, E., Eschrich, W., 1978: Sucrose in the free space of translocating maize leaf bundles. Plant Physiol.62, 491–494.
Kolattukudy, P. E., 1980: Biopolyester membranes of plants: cutin and suberin. Science208, 990–1000.
Knox, R. B., Heslop-Harrison, J., 1970: Direct demonstration of low permeability of the angiosperm meiotic tetrad using a fluorogenic ester. Z. Pflanzenphysiol.62, 451–459.
Kuo, J., O'Brien, T. P., Canny, M. J., 1974: Pit-field distribution, plasmodesmatal frequency, and assimilate flux in the mestome sheath cells of wheat leaves. Planta121, 97–118.
—,Zee, S.-Y., 1972: The transverse veins of the wheat leaf. Aust. J. biol. Sci.25, 721–737.
Laetsch, W. M., 1974: The C4 syndromes: a structural analysis. Ann. Rev. Plant Physiol.25, 27–52.
Läuchli, A., 1976: Apoplastic transport in tissues. In: Encycl. plant physiol. Vol. 2. Transport in plants II B (Lüttge, U., Pitman, M. G., eds.), pp. 4–34. Berlin-Heidelberg-New York: Springer.
Maier-Maercker, U., 1980: “Peristomatal transpiration” and stomatal movement: a controversial view. VI. Lanthanum deposits in the epidermal apoplast. Z. Pflanzenphysiol.100, 121–130.
Nagahashi, G., Thomson, W. W., Leonard, R. T., 1974: The Casparian strip as a barrier to the movement of lanthanum in corn roots. Science183, 670–671.
O'Brien, T. P., Carr, D. J., 1970: A suberized layer in cell walls of the bundle sheath of grasses. Aust. J. biol. Sci.23, 275–287.
—,Kuo, J., 1975: Development of the suberized lamella in the mestome sheath of wheat leaves. Aust. J. Bot.23, 783–794.
Osmond, C. B., Smith, F. A., 1976: Symplastic transport of metabolites during C4-photosynthesis. In: Intercellular communication in plants: Studies on plasmodesmata (Gunning, B. E. S., Robards, A. W., eds.), pp. 229–240. Berlin-Heidelberg-New York: Springer.
Pizzolato, T. D., Burbano, J. L., Berlin, J. D., Morey, P. R., Pease, R. W., 1976: An electron microscope study of the path of water movement in transpiring leaves of cotton (Gossypium hirsutum L.). J. exp. Bot.27, 145–166.
Revel, J. P., Karnovsky, M. J., 1967: Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell Biol.33, C7-C12.
Robards, A. W., Robb, M. E., 1974: The entry of ions and molecules into roots: an investigation using electron-opaque tracers. Planta120, 1–12.
Schönherr, J., Ziegler, H., 1980: Water permeability ofBetula periderm. Planta147, 345–354.
Shaklai, M., Tavassoli, M., 1982: Preferential localization of lanthanum to nuclear-pore complexes. J. Ultrastruct. Res.81, 139–144.
Sitte, P., 1975: Die Bedeutung der molekularen Lamellenbauweise von Korkzellwänden. Biochem. Physiol. Pflanzen168, 287–297.
Soliday, C. L., Kolattukudy, P. E., Davies, R. W., 1979: Chemical and ultrastructural evidence that the waxes associated with the suberin polymer constitute the major diffusion barrier to water vapor in potato tuber (Solanum tuberosum L.). Planta146, 607–614.
Spurr, A. R., 1969: A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res.26, 31–43.
Tanton, T. W., Crowdy, S. H., 1972: Water pathways in higher plants. III. The transpiration stream within leaves. J. exp. Bot.23, 619–625.
Thomson, W. W., Platt, K. A., Campbell, N., 1973: The use of lanthanum to delineate the apoplastic continuum in plants. Cytobios8, 57–62.
Van Steveninck, R. F. M., van Steveninck, M. E., Chescoe, D., 1976: Intracellular binding of lanthanum in root tips of barley (Hordeum vulgare). Protoplasma90, 89–97.
Weiss, G. B., 1974: Cellular pharmacology of lanthanum. Ann. Rev. Pharmacology14, 343–354.
Zee, S.-Y., O'Brien, T. P., 1971: Vascular transfer cells in the wheat spikelet. Aust. J. biol. Sci.24, 35–49.
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Evert, R.F., Botha, C.E.J. & Mierzwa, R.J. Free-space marker studies on the leaf ofZea mays L.. Protoplasma 126, 62–73 (1985). https://doi.org/10.1007/BF01287674
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DOI: https://doi.org/10.1007/BF01287674