Summary
The relative hydraulic conductivities of major and minor longitudinal veins, and the apoplastic permeability of the bundle sheaths surrounding all longitudinal and transverse veins were investigated in representatives of the C3, C4/NAD-ME, C4/NAD-ME/PCK intermediate, C4/PCK and C4/NADP-ME photosynthetic types. Using the Hagen-Poiseuille equation and measurements of tracheary element diameters, the number of elements in each vein type and the numbers of each vein type, we calculated that 87–99% of the water flow in a longitudinal direction would be expected to occur in the major veins. The permeability of the mestome sheaths and parenchymatous bundle sheaths surrounding the veins was tested using the negatively-charged, fluorescent dye, trisodium 3-hydroxy-5,8,10-pyrenetrisulfonate (PTS). This dye proved nontoxic to plant tissue at a concentration of 0.5%, according to a deplasmolysis test with onion epidermal strips. The PTS concentration achieved in the tested grass leaves was about 0.035%, well below the toxic limit. When a solution of PTS was fed to the leaves by means of a basal cut, the dye moved into the veins of all orders. From there, it moved outward into the surrounding tissues, indicating that the sheaths surrounding the veins of all orders in all species tested were permeable. Therefore, contrary to previous predictions based on structural observations and some tracer studies, bundle sheaths with suberized cell walls do not function as endodermal layers.
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References
Altus DP, Canny MJ (1985) Water pathways in wheat leaves I. The division of fluxes between different vein types. Aust J Plant Physiol 12: 173–181
— —,Blackman DR (1985) Water pathways in wheat leaves. II. Water-conducting capacities and vessel diameters of different vein types, and the behaviour of the integrated vein network. Aust J Plant Physiol 12: 183–199
Barnabas AD (1983) Composition and fine structural features of longitudinal veins in leaves ofThalassodendron ciliatum. S Afr J Bot 2: 317–325
Botha CEJ, Evert RF (1986) Free-space marker studies on the leaves ofSaccharum officinarum andBromus unioloides. S Afr J Bot 52: 335–342
Botha CEJ, Evert RF, Cross RHM, Marshall DM (1982) The suberin lamella, a possible barrier to water movement from the veins to the mesophyll ofThemeda triandra Forsk. Protoplasma 112: 1–8
Brisson JD, Peterson RL, Robb J, Rauser WE, Ellis BE (1977) Correlated phenolic histochemistry using light, transmission, and scanning electron microscopy, with examples taken from phytopathological problems. Scanning Electron Microscopy Vol II: 667–676
Brown WV (1958) Leaf anatomy in grass systematics. Bot Gaz 119: 170–178
Burbano JL, Pizzolato TD, Morey PR, Berlin JD (1976) An application of the Prussian Blue technique to a light microscope study of water movement in transpiring leaves of cotton (Gossypium hirsutum L). J Exp Bot 27: 134–144
Byott GS, Sheriff DW (1976) Water movement into and throughTradescantia virginiana (L.) leaves II. Liquid flow and evaporative sites. J Exp Bot 27: 634–639
Canny MJ (1986) Water pathways in wheat leaves. III. The passage of the mestome sheath and the function of the suberised lamellae. Physiol Plant 66: 637–647
—,McCully ME (1986) Locating water-soluble vital stains in plant tissues by freeze-substitution and resin-embedding. J Microscopy 142: 63–70
Carpita N, Sabularse D, Montezinos D, Delmer DP (1979) Determination of the pore size of cell walls of living plant cells. Science 205: 1144–1147
Chonan N (1972) Differences in mesophyll structure between temperate and tropical grasses. Proc Crop Sci Soc Japan 41: 414–419
—,Kawahara H, Matsuda T (1984) Ultrastructure of vascular bundles and fundamental parenchyma in relation to movement of photosynthate in leaf sheath of rice. Jap J Crop Sci 53: 435–444
Clarkson DT, Hanson JB (1980) The mineral nutrition of higher plants. Ann Rev Plant Physiol 31: 239–298
—,Robards AW, Stephens JE, Stark M (1987) Suberin lamellae in the hypodermis of maize (Zea mays) roots; development and factors affecting the permeability of hypodermal layers. Plant Cell Environ 10: 83–93
Crookston RK (1980) The structure and function of C4 vascular plants-some unanswered questions. Ber Deutsch Bot Ges 93: 71–78
Cutter EG (1971) Plant anatomy: experiment and interpretation part 2. Organs. Edward Arnold Publishers Ltd, London
Dengler NG, Dengler RE, Hattersley PW (1985) Differing ontogenetic origins of PCR (“Kranz”) sheaths in leaf blades of C4 grasses (Poaceae). Amer J Bot 72: 284–302
Dybing CD, Currier HB (1959) A fluorescent dye method for foliar penetration studies. Weeds 7: 214–222
— — (1961) Foliar penetration by chemicals. Plant Physiol 36: 169–174
Eastman PAK, Dengler NG, Peterson CA (1988) Suberized bundle sheath in grasses (Poaceae) of different photosynthetic types. I. Anatomy, ultrastructure and histochemistry. Protoplasma 142: 92–111
Eleftheriou EP, Tsekos I (1979) Development of mestome sheath cells in leaves ofAegilops comosa varthessalica. Protoplasma 100: 139–153
Esau K (1977) Anatomy of seed plants, 2nd edn. John Wiley and Sons, New York
Evert RF, Botha CEJ, Mierzwa RJ (1985) Freespace marker studies in the leaf ofZea mays L. Protoplasma 126: 62–73
—,Eschrich W, Heyser W (1977) Distribution and structure of the plasmodesmata in mesophyll and bundle-sheath cells ofZea mays L. Planta 136: 77–89
Fahn A (1974) Plant anatomy. Pergamon Press, Oxford
Fischer JMC, Peterson CA, Bols NC (1985) A new fluorescent test for cell vitality using Calcofluor White M2R. Stain Technol 60: 69–79
Gaff DF, Chambers TC, Markus K (1964) Studies of extrafascicular movement of water in the leaf. Aust J Biol Sci 17: 581–586
Griffith M, Huner NPA, Espelie KE, Kolattukudy PE (1985) Lipid polymers accumulate in the epidermis and mestome sheath cell walls during low temperature development of winter rye leaves. Protoplasma 125: 53–64
Hanson PJ (1983) Apoplastic water flux through the root systems ofPinus resinosa Ait. seedlings. MSc Thesis, University of Minnesota
—,Sucoff EI, Markhart III AH (1985) Quantifying apoplastic flux through red pine root systems using trisodium, 3-hydroxy-5,8,10-pyrenetrisulphonate. Plant Physiol 77: 21–24
Harris PJ, Hartley RD (1976) Detection of bound ferulic acid in cell walls of the Gramineae by ultraviolet fluorescence microscopy. Nature 259: 508–510
— — (1980) Phenolic constituents of the cell walls of monocotyledons. Biochem System Ecol 8: 153–160
Hartley RD, Jones EC (1977) Phenolic components and degradability of cell walls of grass and legume species. Phytochemistry 16: 1531–1534
Hattersley PW, Browning AJ (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
—,Wong SC, Perry S, Roksandic Z (1986) Comparative ultrastructure and gas exchange characteristics of the C3–C4 intermediateNeurachne minor S. T.Blake (Poaceae). Plant Cell Environ 9: 217–233
Holloway PJ (1983) Some variations in the composition of suberin from the cork layers of higher plants. Phytochemistry 22: 495–502
Kemp PR, Cunningham GG, Adams HP (1983) Specialization of mesophyll morphology in relation to C4 photosynthesis in thePoaceae. Amer J Bot 70: 349–354
Kolattukudy PE (1980) Cutin, suberin, and waxes In:Stumpf PK (ed) The biochemistry of plants, Vol. 4 Lipids: structure and function. Academic Press, New York, p 571–645
— (1985) Biochemistry and function of cutin and suberin. Can J Bot 62: 2918–2933
Kuo J, O'Brien TP, Zee S-Y (1972) The transverse veins of the wheat leaf. Aust J Biol Sci 25: 721–737
— —,Canny MJ (1974) Pit-field distribution, plasmodesmatal frequency, and assimilate flux in the mestome sheath cells of wheat leaves. Planta 121: 97–118
LÄuchli A (1976) Apoplasmic transport in tissue. In: Encyclopedia of plant physiology, New Series, Vol 2B Transport in plants II. Springer, Berlin Heidelberg New York, pp 3–33
Lüttge U, Higinbotham N (1979) Transport in plants. Springer, Berlin Heidelberg New York, p 84–85
Martin RB, Richardson FS (1979) Lanthanides as probes for calcium in biological systems. Quart Rev Biophys 12: 181–209
Moon GJ, Clough BF, Peterson CA, Allaway WG (1986) Apoplastic and symplastic pathways inAvicennia marina (Forsk.) Vierh. roots revealed by fluorescent tracer dyes. Aust J Plant Physiol 13: 637–648
Nimz HH, Robert D, Farx O, Nemr M (1981) Carbon-13 NMR spectra of lignins, 8 structural differences between lignins of hardwoods, softwoods, grasses and compression wood. Holzforschung 35: 16–26
O'Brien TP, Carr DJ (1970) A suberized layer in the cell walls of the bundle sheath of grasses. Aust J Biol Sci 23: 275–287
Parker ML, Ford MA (1982) The structure of the mesophyll of flag leaves in threeTriticum species. Ann Bot 49: 165–176
Patel KM (1964) Absorption of two fluorescent dyes by roots of detopped barley plants. MSc Thesis, University of California, Davis
Peterson CA, Edgington LV (1976) Entry of pesticides into the plant symplast as measured by their loss from an ambient solution. Pestic Sci 7: 483–491
—,Emmanuel ME, Humphreys GB (1981) Pathway of movement of apoplastic fluorescent dye tracers through the endodermis at the site of secondary root formation in corn (Zea mays) and broad bean (Vicia faba). Can J Bot 59: 618–625
—,Griffith M, Huner NPA (1985) Permeability of the suberized mestome sheath in winter rye. Plant Physiol 77: 157–161
Prendergast HDV, Hattersley PW, Stone NE, Lazarides Z (1986) C4 acid decarboxylation type inEragrostis (Poaceae): patterns of variation in chloroplast position, ultrastructure and geographical distribution. Plant Cell Environ 9: 333–344
Riley RG, Kolattukudy PE (1975) Evidence for covalently attached p-coumaric acid and ferulic acid in cutins and suberin. Plant Physiol 56: 650–654
Robards AW, Robb ME (1974) The entry of ions and molecules into roots: an investigation using electron opaque tracers. Planta 120: 1–12
—,Clarkson DT, Sanderson J (1979) Structure and permeability of the epidermal/hypodermal layers of the sand sedge (Carex arenaria, L.). Protoplasma 101: 331–347
Ryser U, Meier H, Holloway PJ (1983) Identification and localization of suberin in the cell walls of green cotton fibres (Gossypium hirsutum L., var. green lint). Protoplasma 117: 196–205
Salisbury FB, Ross CW (1978) Plant physiology, 2nd ed. Wadsworth Publishing, Belmont CA, p 98
Schwendener S (1890) Die Mestomscheiden der GrÄmineenblÄtter. Sitzungsber Preuss Akad Wiss Phys-Math Kl 22: 405–426
Shaklai M, Tavassoli M (1982) Preferential localization of lanthanum to nuclear pore complexes. J Ultrastruct Res 81: 139–144
Spurr AR (1969) A low viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26: 31–43
Stroshine L, Cooke JR, Rand RH, Cutler JM, Chabot JF (1979) Mathematical analysis of pressure chamber efflux curves. Proc Amer Soc Agric Eng, Paper No 79-4585, pp 1–45
—,Rand RH, Cooke JR, Cutler JM, Chabot JF (1985) An analysis of resistance to water flow through wheat and tall fescue leaves during pressure chamber efflux experiments. Plant Cell Environ 8: 7–18
Strugger S (1940) Studien über den Transpirationsstrom im Blatt vonSecale cereale undTriticum vulgare. Z Bot 35: 97–113
—,Peveling E (1961) Die electronenmikroskopische Analyse der extrafaszikulÄren Komponente des Transpirationsstromes mit Hilfe von Edelmetallsuspensoiden adÄquater DispersitÄt. Ber Deutsch Bot Ges 74: 300–304
Tanton TW, Crowdy SH (1972) Water pathways in higher plants III. The transpiration stream within leaves. J Exp Bot 23: 619–625
Thompson WW, Platt KA, Campbell N (1973) The use of lanthanum to delineate the apoplastic continuum in plants. Cytobios 8: 57–62
Turnbull JR (1980) Histochemistry and microspectrophotometry of plant phenolics usingColeus blumei suspension cultures as a model system. MSc Thesis, University of Guelph, Canada
Van Fleet DS (1950) The cell forms, and their common substance reactions, in the parenchyma-vascular boundary. Bull Torr Bot Club 77: 340–353
Westgate ME, Steudle E (1985) Water transport in the midrib tissue of maize leaves. Direct measurement of the propagation of changes in cell turgor across a plant tissue. Plant Physiol 78: 183–191
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Eastman, P.A.K., Peterson, C.A. & Dengler, N.G. Suberized bundle sheaths in grasses (Poaceae) of different photosynthetic types. II. Apoplastic permeability. Protoplasma 142, 112–126 (1988). https://doi.org/10.1007/BF01290868
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DOI: https://doi.org/10.1007/BF01290868