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Ultrastructural indications for coexistence of symplastic and apoplastic phloem loading in Commelina benghalensis leaves

Differences in ontogenic development, spatial arrangement and symplastic connections of the two sieve tubes in the minor vein

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Abstract

The ultrastructural ontogeny of Commelina benghalensis minor-vein elements was followed. The mature minor vein has a restricted number of elements: a sheath of six to eight mestome cells encloses one xylem vessel, three to five vascular parenchyma cells, a companion cell, a thin-walled protophloem sieve-tube member and a thick-walled metaphloem sieve-tube member. The protophloem sieve-tube member (diameter 4–5 μm; wall thickness 0.12 μm) and the companion cell originated from a common mother cell. The metaphloem sieve-tube member (diameter 3 μm; wall thickness 0.2 μm) developed from the same precursor cell as the phloem parenchyma cells. Counting the plasmodesmatal frequencies demonstrated a symplastic continuum from mesophyll to the minor-vein phloem. The metaphloem sievetube member and the phloem parenchyma cells are the termini of this symplast. The protophloem sieve-tube member and companion cell constitute an insulated symplastic domain. The symplastic route, mesophyll to metaphloem sieve tube, appears to offer a path for symplastic loading; the protophloem sieve tube may be capable of accumulation from the apoplast. A similar two-way system of loading may exist in a number of plant families. Plasmodesmograms (a novel way to depict cell elements, plasmodesmatal frequencies and vein architecture) of some other species also displayed the anatomical requirements for two routes from mesophyll to sieve tube and indicate the potential coexistence of symplastic and apoplastic loading.

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References

  • Altus, D.P., Canny, M.J. (1985) Loading of assimilates in wheat leaves. II. The path from chloroplast to vein. Plant Cell Environ 8, 275–285

    Google Scholar 

  • Behnke, H.D. (1973) Plastids in sieve elements and their companion cells. Investigations on monocotyledons with special reference to Smilax and Tradescantia. Planta 110, 321–328

    Google Scholar 

  • Behnke, H.D. (1983) Cytology and morphogenesis of higher plant cells. Phloem. Prog. Bot. 45, 18–35

    Google Scholar 

  • 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 of Themeda triandra Forsk. Protoplasma 112, 1–8

    Google Scholar 

  • Cataldo, D.A. (1974) Vein loading: the role of the symplast in intercellular transport of carbohydrate between the mesophyll and the minor veins of tobacco. Plant Physiol. 53, 912–917

    Google Scholar 

  • Delrot, S. (1987) Phloem loading: apoplastic or symplastic? Plant Physiol. Biochem. 25, 667–676

    Google Scholar 

  • Eleftheriou, E.P., Tsekos, I. (1979) Development of mestome sheath cells in leaves of Aegilops comosa var. thessalica. Protoplasma 100, 139–153

    Google Scholar 

  • Erwee, M.G., Goodwin, P.B. (1983) Characterization of the Egeria densa symplast: inhibition of the intercellular movement of fluorescent probes by group II ions. Planta 158, 320–328

    Google Scholar 

  • Erwee, M.G., Goodwin, P.B., Van Bel, A.J.E. (1985) Cell-to-cell communication in the leaves of Commelina cyanea and other plants. Plant Cell Environ 8, 173–178

    Google Scholar 

  • Evert, R.F., Botha, C.E.J., Mierzwa, R.J. (1985) Free-space marker studies on the leaf of Zea mays L. Protoplasma 126, 62–73

    Google Scholar 

  • Evert, R.F., Eschrich, W., Heyser, W. (1977) Distribution and structure of the plasmodesmata in the mesophyll and bundle-sheath cells of Zea mays L. Planta 136, 77–89

    Google Scholar 

  • Evert, R.F., Eschrich, W., Heyser, W. (1978) Leaf structure in relation to solute transport and phloem loading in Zea mays L. Planta 138, 279–294

    Google Scholar 

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

    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., 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 

  • Fritz, E., Evert, R.F., Heyser, W. (1983) Microautoradiographic studies of phloem loading and transport in the leaf of Zea mays L. Planta 159, 193–206

    Google Scholar 

  • Gamalei, Y.V. (1985) Characteristics of phloem loading in woody and herbaceous plants. Sov. Plant. Physiol. 32, 656–665

    Google Scholar 

  • Gamalei, Y.V., Pakhomova, M.V. (1981) Distribution of plasmodesmata and parenchyma transport of assimilates in the leaf of several dicots. Fiziol. Rast. 28, 901–912

    Google Scholar 

  • Geiger, D.R., Giaquinta, R.T., Sovonick, S.A., Fellows, R.J., (1973) Solute distribution in sugar beet leaves in relation to phloem loading and translocation. Plant Physiol. 52, 585–589

    Google Scholar 

  • Geiger, D.R., Sovonick, S.A., Shock, T.L., Fellows, R.J. (1974) Role of free space in translocation in sugar beet. Plant Physiol. 54, 892–898

    Google Scholar 

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

    Google Scholar 

  • Goodwin, P.B. (1983) Molecular size limits for movement in the symplast of the Elodea leaf. Planta 157, 124–130

    Google Scholar 

  • Gunning, B.E.S. (1976) The role of plasmodesmata in short distance transport to and from the phloem. In: Intercellular communication in plants: studies of plasmodesmata, pp. 203–277, Gunning, B.E.S., Robards, A.W., eds. Springer, Berlin Heidelberg Tokyo New York

    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. Bot. 28, 87–126

    Google Scholar 

  • 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. Protoplasma 109, 371–401

    Google Scholar 

  • Ho, L.C., Baker, D.A. (1982) Regulation of loading and unloading in long distance transport systems. Physiol. Plant. 56, 225–230

    Google Scholar 

  • Kuo, J., O'Brien, T.P. (1974) Lignified sieve elements in the wheat leaf. Planta 117, 349–353

    Google Scholar 

  • Kuo, J., O'Brien, T.P., Canny, M.J., (1974) Pit-field distribution, plasmodesmatal frequency, assimilate flux in the mestome sheath cells of wheat leaves. Planta 121, 97–118

    Google Scholar 

  • Madore, M.A., Lucas, W.J. (1987) Control of photoassimilate movement in source-leaf tissues of Ipomoea tricolor Cav. Planta 171, 197–204

    Google Scholar 

  • Madore, M.A., Oross, J.W., Lucas, W.J. (1986) Symplastic transport in Ipomoea tricolor source leaves. Demonstration of functional symplastic connections from mesophyll to minor veins by a novei dye-tracer method. Plant Physiol. 82, 432–442

    Google Scholar 

  • Madore, M.A., Webb, J.A. (1981) Leaf free space and analysis and vein loading in Cucurbita pepo. Can. J. Bot. 59, 2550–2557

    Google Scholar 

  • Maynard, J.W., Lucas, W.J. (1982) Sucrose and glucose uptake into Beta vulgaris leaf tissues. A case for general (apoplastic) retrieval systems. Plant Physiol. 70 1436–1445

    Google Scholar 

  • Miyake, T.H., Maeda, E. (1976) The fine structure of plastids in various tissues in the leaf blade of rice. Ann. Bot. 40, 1131–1140

    Google Scholar 

  • O'Brien, T.P., Kuo, J. (1975) Development of the suberized lamella in the mestome sheath of wheat. Aust. J. Bot. 23, 783–794

    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, C.A., Griffith, M., Huner, N.P.A. (1985) Permeability of the suberized mestome sheath in winter rye. Plant Physiol. 77, 157–161

    Google Scholar 

  • Peterson, R.L., Yeung, E.C. (1975) Ontogeny of phloem transfer cells in Hieracium floribundum. Can. J. Bot. 43, 2745–2758

    Google Scholar 

  • Russin, W., 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 

  • Schmitz, K., Cuypers, B., Moll, M. (1987) Pathway and assimilate transfer between mesophyll cells and minor veins in leaves of Cucumis melo L. Planta 171, 19–29

    Google Scholar 

  • Turgeon, R., Webb, J.A. (1976) Leaf development and phloem transport in Cucurbita pepo: maturation of the minor veins. Planta 129, 265–269

    Google Scholar 

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

    Google Scholar 

  • Van Bel, A.J.E. (1986) Amino acid loading by minor veins of Commelina benghalensis: an integration of structural and physiological aspects. In: Fundamental, ecological and agricultural aspects of nitrogen fixation in higher plants, pp. 111–114, Lambers, H., Neeteson, J.J., Stulen, I., eds. Martinus Nijhoff Publishers, Dordrecht

    Google Scholar 

  • Van Bel, A.J.E. (1987) The apoplast concept of phloem loading has no universal validity. Plant Physiol. Biochem. 25, 677–686

    Google Scholar 

  • Van Bel, A.J.E., Ammerlaan, A., Blaauw-Jansen, G. (1986) Preferential accumulation by mesophyll cells at low and by veins at high exogenous amino acid and sugar concentrations in Commelina benghalensis L. leaves. J. Exp. Bot. 37, 1899–1910

    Google Scholar 

  • Van Bel, A.J.E., Koops, A.J. (1985) Uptake of 14C-sucrose in isolated minor vein networks of Commelina benghalensis L. Planta 164, 362–369

    Google Scholar 

  • Van Kesteren, W.J.P., Van der Schoot, C., Van Bel, A.J.E. (1988) Symplastic transfer of fluorescent dyes from mesophyll to sieve tube in stripped leaf tissue and partly isolated minor veins of Commelina benghalensis. Plant Physiol., in press

  • Walsh, M.A. (1974) Late-formed metaphloem sieve elements in Zea mays. L. Planta 121, 17–25

    Google Scholar 

  • Wang, X.D., Canny, M.J. (1985) Loading and translocation of assimilates in the fine veins of sunflower leaves. Plant Cell Environ 8, 669–685

    Google Scholar 

  • Wilson, C., Oross, J.W., Lucas, W.J. (1985) Sugar uptake into Allium cepa leaf tissue: an integrated approach. Planta 164, 227–240

    Google Scholar 

  • Ziegler, H. (1971) Wasserumsatz und Stoffbewegungen. Fortschr. Bot. 33, 63–84

    Google Scholar 

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Authors and Affiliations

  1. Transport Physiology Research Group, Botanical laboratory, University of Utrecht, Lange Nieuwstraat 106, NL-3512 PN, Utrecht, The Netherlands

    A. J. E. van Bel, W. J. P. van Kesteren & C. Papenhuijzen

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  1. A. J. E. van Bel
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  2. W. J. P. van Kesteren
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  3. C. Papenhuijzen
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van Bel, A.J.E., van Kesteren, W.J.P. & Papenhuijzen, C. Ultrastructural indications for coexistence of symplastic and apoplastic phloem loading in Commelina benghalensis leaves. Planta 176, 159–172 (1988). https://doi.org/10.1007/BF00392441

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  • DOI: https://doi.org/10.1007/BF00392441

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