Skip to main content
SpringerLink
Log in

Transfer cells and solute uptake in minor veins of Pisum sativum leaves

  • Published:
Planta Aims and scope Submit manuscript

Abstract

Morphometric and physiological studies were conducted to determine whether the wall ingrowths of transfer cells in the minor-vein phloem of Pisum sativum L. leaves increase the capacity of the cells for solute influx. Size and number of wall ingrowths are positively correlated to the photon flux density (PFD) at which the plants are grown. An analysis of plasmodesmatal frequencies indicated that numerous plasmodesmata are present at all interfaces except those between the sieveelement-transfer-cell complex (SE-TCC) and surrounding cells where plasmodesmata are present but few in number. Flux of exogenous sucrose into the SE-TCC was estimated from kinetic profiles of net sucrose influx into leaf discs, quantitative autoradiography, and measurements of sucrose translocation. Flux based both on the saturable (carrier-mediated) and the linear components of influx was 47% greater in leaves of plants grown at high PFD (1000 μmol·m−2·s−1) than those grown in low PFD (200 μmol·m−2·s−1) and was paralleled by a 47% increase in SE-TCC plasmalemma surface area. Flux of endogenous photosynthate across the SE-TCC plasmalemma was calculated from carbon balance and morphometric data. The increase in flux in high-light leaves over that in low-light leaves can be explained on the basis of an increase in plasmalemma surface area. In intact leaves, a ‘standing osmotic gradient’ may facilitate transport of solute into transfer cells with extensive wall elaborations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

LPI:

leaf plastochron index

PCMBS:

p-chloromercuribenzenesulfonic acid

PFD(s):

photon flux density (densities)

SE-TCC:

sieve-element-transfer-cell complex

References

  • Bentwood, B.J., Cronshaw, J. (1978) Cytochemical localization of adenosine triphosphatase in the phloem of Pisum sativum and its relation to the function of transfer cells. Planta 140, 111–120

    Google Scholar 

  • Bourquin, S., Bonnemain, J.-L., Delrot, S. (1990) Inhibition of loading of 14C assimilates by p-chloromercuribenzenesulfonic acid. Localization of the apoplastic pathway in Vicia faba. Plant Physiol. 92, 97–102

    Google Scholar 

  • Daniel, W.W. (1978) Biostatistics: a foundation for analysis in the health sciences, 2nd edn. Wiley, New York

    Google Scholar 

  • Ding, B., Parthasarathy, M.V., Turgeon, R. (1988) A morphometric analysis of the phloem-unloading pathway in developing tobacco leaves. Planta 176, 307–318

    Google Scholar 

  • Erickson, R.O., Michelini, F.J. (1957) The plastochron index. Am. J. Bot. 44, 297–305

    Google Scholar 

  • Evert, R.F., Mierzwa, R.J. (1986) Pathway(s) of assimilate movement from mesophyll cells to sieve tubes in the Beta vulgaris leaf. In: Plant biology, vol. 1: Phloem transport, pp. 419–432, Cronshaw, J., Lucas, W.J., Giaquinta, R.T., eds. Alan R. Liss, New York

    Google Scholar 

  • Faraday, C.D., Thomson, W.W. (1986) Structural aspects of the salt glands of the Plumbaginaceae. J. Exp. Bot. 37, 461–470

    Google Scholar 

  • Fisher, D.G. (1986) Ultrastructure, plasmodesmatal frequency, and solute concentration in green areas of variegated Coleus blumei Benth. leaves. Planta 169, 141–152

    Google Scholar 

  • Fisher, D.G. (1990) Distribution of plasmodesmata in leaves. A comparison of Cananga odorata with other species using different measures of plasmodesmatal frequency. In: Parallels in cell to cell junctions in plants and animals, pp. 199–221, Robards, A.W., ed. Springer-Verlag, Berlin Heidelberg

    Google Scholar 

  • Fisher, D.G., Evert, R.F. (1982) Studies on the leaf of Amaranthus retroflexus (Amaranthaceae): ultrastructure, plasmodesmatal frequency, and solute concentration in relation to phloem loading. Planta 155, 377–387

    Google Scholar 

  • Folsom, M.W., Cass, D.D. (1986) Changes in transfer cell distribution in the ovule of soybean after fertilization. Can. J. Bot. 64, 965–972

    Google Scholar 

  • Folsom, M.W., Peterson, C.M. (1984) Ultrastructural aspects of the mature embryo sac of soybean, Glycine max (L.) Merr. Bot. Gaz. 145, 1–10

    Google Scholar 

  • Fondy, B.R., Geiger, D.R. (1982) Diurnal pattern of translocation and carbohydrate metabolism in source leaves of Beta vulgaris L. Plant Physiol. 70, 671–676

    Google Scholar 

  • Gamalei, Y.V. (1985a) Plasmodesmata: intercellular communication in plants. [In russ.] Fiziol. Rast. 32, 176–190

    Google Scholar 

  • Gamalei, Y.V. (1985b) Characteristics of phloem loading in woody and herbaceous plants. [In Russ.] Fiziol. Rast. 32, 866–875

    Google Scholar 

  • Giaquinta, R.T. (1983) Phloem loading of sucrose. Annu. Rev. Plant Physiol. 34, 347–387

    Google Scholar 

  • Gordon, A.J. (1986) Diurnal patterns of photosynthate allocation and partitioning among sinks. In: Phloem transport, pp. 499–517, Cronshaw, J., Lucas, W.J., Giaquinta, R.T., eds. Alan R. Liss, New York

    Google Scholar 

  • Gunning, B.E.S., Pate, J.S. (1969) “Transfer cells” plant cells with wall ingrowths, specialized in relation to short distance transport of solutes — their occurrence, structure, and development. Protoplasma 68, 107–133

    Google Scholar 

  • Gunning, B.E.S., Pate, J.S. (1974) Transfer cells. In: Dynamic aspects of plant ultrastructure, pp. 441–480, Robards, A.W., ed. McGraw-Hill, London, New York

    Google Scholar 

  • Gunning, B.E.S., Pate, J.S., Briarty, L.G. (1968) Specialized “transfer cells” in minor veins of leaves and their possible significance in phloem translocation. J. Cell Biol. 37, C7–12

    Google Scholar 

  • Gunning, B.E.S., Pate, J.S., Minchin, F.R., Marks, I. (1974) Quantitative aspects of transfer cell structure in relation to vein loading in leaves and solute transport in legume nodules. Symp. Soc. Exp. Biol. 28, 87–126

    Google Scholar 

  • Hill, A.E. (1975a) Solute-solvent coupling in epithelia; a critical examination of the standing-gradient osmotic flow theory. Proc. R. Soc. London Ser. B 190, 99–114

    Google Scholar 

  • Hill, A.E. (1975b) Solute-solvent coupling in epithelia; an electro-osmotic theory of fluid transfer. Proc. R. Soc. London Ser. 190, 115–134

    Google Scholar 

  • Huber, S.C., Kerr, P.S., Kalt-Torres, W. (1985) Regulation of sucrose formation and movement. In: Regulation of carbon partitioning in photosynthetic tissue, pp 199–214, Heath, R.L., Preiss, J., eds. American Society of Plant Physiologists, Rockville, Md., USA

    Google Scholar 

  • Kramer, D., Anderson, W.P., Preston, J. (1978) Transfer cells in the root epidermis of Atriplex hastata L. as a response to salinity: a comparative cytological and X-ray microprobe investigation. Aust. J. Plant Physiol. 5, 739–747

    Google Scholar 

  • Kronestedt, E.C., Robards, A.W. (1987) Sugar secretion from the nectary of Strelitzia: an ultrastructural and physiological study. Protoplasma 137, 168–182

    Google Scholar 

  • Kuo, J. (1983) The nacreous walls of sieve elements in seagrasses. Am. J. Bot. 70, 159–164

    Google Scholar 

  • Landsberg, E.C. (1982) Transfer cell formation in the root epidermis: a prerequisite for Fe-efficiency? J. Plant Nutr. 5, 415–432

    Google Scholar 

  • Maier, K., Maier, U. (1972) Localization of beta-glycerophosphatase and Mg++-activated adenosine triphosphatase in a moss haustorium, and the relation of these enzymes to the cell wall labyrinth. Protoplasma 75, 91–112

    Google Scholar 

  • Maynard, J.W., Lucas, W.J. (1982) A reanalysis of the two-component phloem loading system in Beta vulgaris. Plant Physiol. 69, 734–739

    Google Scholar 

  • Maze, J., Lin, S.C. (1975) A study of the mature megagametophyte of Stipa elmeri. Can. J. Bot. 53, 2958–2977

    Google Scholar 

  • Pate, J.S. (1966) Photosynthesizing leaves and nodulated roots as donors of carbon to protein of the shoot of the field pea (Pisum arvense L). Ann. Bot. 30, 93–109

    Google Scholar 

  • Pate, J.S., Gunning, B.E.S. (1969) Vascular transfer cells in Angiosperm leaves: A taxonomic and morphological survey. Protoplasma 68, 135–156

    Google Scholar 

  • Peterson, R.L., Yeung, E.C. (1975) Ontogeny of phloem transfer cells in Hieracium floribundum. Can. J. Bot. 53, 2745–2758

    Google Scholar 

  • Renault, S., Despeghel-Caussin, C., Bonnemain, J.-L., Delrot, S. (1989) The proton electrochemical transmembrane gradients generated by the transfer cells of the haustorium of Polytrichum formosum and their use in the uptake of amino acids. Plant Physiol. 90, 913–920

    Google Scholar 

  • Robards, A.W. (1976) Plasmodesmata in higher plants. In: Intercellular communication in plants: studies on plasmodesmata, pp. 15–57, Gunning, B.E.S., Robards, A.W., eds. Springer, Berling Heidelberg New York

    Google Scholar 

  • Russin, W.A., Evert, R.F. (1985) Studies on the leaf of Populus deltoides (Salicaceae): ultrastructure, plasmodesmatal frequency and solute concentrations. Am. J. Bot. 72, 1232–1247

    Google Scholar 

  • Scheirer, D.C. (1983) Leaf parenchyma with transfer cell-like characteristics in the moss, Polytrichum commune Hedw. Am. J. Bot. 70, 987–992

    Google Scholar 

  • Schmalstig, J.G., Geiger, D.R. (1985) Phloem unloading in developing leaves of sugar beet. I. Evidence for pathway through the symplast. Plant Physiol. 79, 237–241

    Google Scholar 

  • Schnepf, E. (1974) Gland cells. In: Dynamic aspects of plant ultrastructure, pp. 331–357, Robards, A.W., ed. McGraw-Hill, London, New York

    Google Scholar 

  • Sovonick, S.A., Geiger, D.R., Fellows, R.J. (1974) Evidence for active phloem loading in the minor veins of sugar beet. Plant Physiol. 54, 886–891

    Google Scholar 

  • Spurr, A.R. (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26, 31–43

    Google Scholar 

  • Sun, D., Wimmers, L.E., Turgeon, R. (1988) Scintillation counting of 14C-labeled soluble and insoluble compounds in plant tissues. Anal. Biochem. 169, 424–427

    Google Scholar 

  • Tilton, V.R., Wilcox, L.W., Palmer, R.G. (1984) Postfertilization wandlabrinthe formation and function in the central cell of soybean, Glycine max (L.) Merr. (Leguminosae). Bot. Gaz. 145, 334–339

    Google Scholar 

  • Turgeon, R. (1987) Phloem unloading in tobacco sink leaves: insensitivity to anoxia indicates a symplastic pathway. Planta 171, 73–81

    Google Scholar 

  • Turgeon, R. (1989) The sink-source transition in leaves. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 119–138

    Google Scholar 

  • Turgeon, R., Beebe, D.U. (1991) The evidence for symplastic phloem loading. Plant Physiol. 96, 349–354

    Google Scholar 

  • Turgeon, R., Wimmers, L.E. (1988) Different patterns of vein loading of exogenous [14C] sucrose in leaves of Pisum sativum and Coleus blumei. Plant Physiol. 87, 179–182

    Google Scholar 

  • Turgeon, T., Webb, J.A., Evert, R.F. (1975) Ultrastructure of minor veins of Curcurbita pepo leaves. Protoplasma 83, 217–232

    Google Scholar 

  • Watson, L., Pate, J.S., Gunning, B.E.S. (1977) Vascular transfer cells in leaves of Leguminosae-Papilionoideae. Bot. J. Linn. Soc. 74, 123–130

    Google Scholar 

  • Willemse, M.T.M., Kapil, R.N. (1981) Antipodals of Gasteria verrucosa (Liliaceae) — an ultrastructural study. Acta. Bot. Neerl. 30, 25–32

    Google Scholar 

Download references

Author information

Author notes

  1. Larry E. Wimmers

    Present address: Department of Vegetable Crops, University of California, 95616, Davis, CA, USA

Authors and Affiliations

  1. Section of Plant Biology, Division of Biological Sciences, Cornell University, 14853, Ithaca, NY, USA

    Larry E. Wimmers & Robert Turgeon

Authors
  1. Larry E. Wimmers
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert Turgeon
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

This research was supported by National Science Foundation Grant DCB-9104159, U.S. Department of Agriculture Competitive Grant 90000854, and Hatch funds.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wimmers, L.E., Turgeon, R. Transfer cells and solute uptake in minor veins of Pisum sativum leaves. Planta 186, 2–12 (1991). https://doi.org/10.1007/BF00201491

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00201491

Key words

Search

Navigation