Journal of Experimental Botany, Vol. 53, No. 366, pp. 131-138,
January 1, 2002
© 2002 Oxford University Press
Original Papers |
Mucilages and polysaccharides in Ziziphus species (Rhamnaceae): localization, composition and physiological roles during drought-stress
1 Horticulture Research International, Wellesbourne, Warwick CV35 9EF, UK
2 Botany Department, The University of Western Australia, Nedlands, WA 6907, Australia
3 Institute of Ecology and Conservation Biology, Althanstrasse 14, A-1090 Vienna, Austria
4 Department of Biological Sciences, University of Dundee, Dundee DD1 4HN, UK
Received 15 April 2001; Accepted 21 August 2001
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResults and discussionConclusionReferences |
|---|
The drought-tolerant tree species Ziziphus mauritiana Lamk. and Z. rotundifolia Lamk. were shown to have similar high mucilage concentrations (7–10% dry weight) in their leaves, with large numbers of mucilage-containing cells in the upper epidermis and extracellular mucilage-containing cavities in the leaf veins and stem cortex. The main sugar constituents of the water-soluble mucilage extract were rhamnose, glucose and galactose. During drought-stress in two independent studies, foliar mucilage content was unaffected in both species, but glucose and starch contents declined significantly in crude mucilage extracts from droughted leaves. Enzymatic hydrolysis of the mucilage extract using
-amylase and amyloglucosidase released glucose, indicating that a mucilage-associated water-soluble glucan, with -1,4- and -1,6-linkages, may exist which was extracted together with the mucilage. From the current data, it is not possible to localize the glucan to determine whether or not it is associated with mucilage-containing cells. Data from pressure–volume analyses of drought-stressed and control leaves showed that, in line with their similar mucilage contents, the relative leaf capacitance isotherm (change in relative water content per unit change in water potential) was similar in both species. During drought-stress, reduced relative capacitance resulted from osmotic adjustment and decreased wall elasticity. Data suggest that in Ziziphus leaves, intracellular mucilages play no part in buffering leaf water status during progressive drought. In Ziziphus species, growing in environments with erratic rainfall, the primary role of foliar mucilage and glucans, rather than as hydraulic capacitors, may be as sources for the remobilization of solutes for osmotic adjustment, thus enabling more effective water uptake and assimilate redistribution into roots and stems prior to defoliation as the drought-stress intensified. Key words: Drought, mucilage, polysaccharides, water relations, Ziziphus.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResults and discussionConclusionReferences |
|---|
Polysaccharide hydrocolloids including mucilages, gums and glucans are abundant in nature and are commonly found in many higher plants. These polysaccharides constitute a structurally diverse class of biological macromolecules with a broad range of physicochemical properties which are widely used for applications in pharmacy and medicine (Franz, 1989
).
Although mucilages can occur in high concentrations in different plant organs, their physiological function in most cases is unclear. Mucilages found in rhizomes, roots and seed endosperms may act primarily as energy reserves (Franz, 1979) whereas foliar mucilages appear not to serve as storage carbohydrates (Diestelbarth and Kull, 1985). Generally, it has been assumed that foliar mucilages are merely secondary plant metabolites (Naglschmid et al., 1982), but there are reports that they may play a role in frost tolerance (Goldstein and Nobel, 1991; Lipp et al., 1994), water transport (Zimmermann et al., 1994), wound responses (Clarke et al., 1979), plant host–pathogen interactions (Davis et al., 1986), the ionic balance of plant cells (Pollak and Albert, 1990; Trachtenberg and Mayer, 1982), and as carbohydrate reserves (Pimienta-Barrios and Nobel, 1998).
Due to the high concentration of hydroxyl groups in the polysaccharide, mucilages generally have a high water-binding capacity and this has led to studies of their role in plant water relations. It has been suggested that the ability of mucilage to hydrate may offer a mechanism for plants to resist drought (Clarke et al., 1979). There is growing evidence that, due to the high water-holding capacity of the polysaccharide, extracellular mucilages in particular may play an important role in the drought resistance of certain plant species (Goldstein and Nobel, 1991; Morse, 1990; Nobel et al., 1992). In Hemizonia luzifolia, extracellular mucilages have been demonstrated to buffer leaf water status against environmental fluctuation during the middle of the day (Morse, 1990). By acting as an apoplastic capacitor (Nobel et al., 1992), mucilages can also enable leaves to maintain water potential when soil water deficits develop (Robichaux and Morse, 1990).
Mucilaginous substances have been reported as occurring widely in the Rhamnaceae, including the genus Ziziphus (Metcalf and Chalk, 1950). However, previous reports on mucilaginous cells in leaf and stem material of Ziziphus have not addressed the abundance, localization, chemical characteristics or potential role of mucilages in this genus (Metcalf and Chalk, 1950).
Trees and shrubs of Ziziphus are characteristically found in many semi-arid regions of the world and can thrive in water-limited environments which may be unsuitable for other forms of annual crop cultivation (Jawanda and Bal, 1978).
Recently, research into the mechanisms for drought tolerance and avoidance in Ziziphus species has shown that Z. mauritiana and Z. rotundifolia exhibit a range of drought avoidance adaptations to progressive drought-stress. Under well-irrigated conditions, Ziziphus mauritiana exhibited high rates of net photosynthesis and transpiration compared to other fruit tree species (Clifford et al., 1997), but during early stages of drought-stress, the stomata were very sensitive to water deficit and reduced stomatal conductance effectively increased intrinsic water use efficiency in the short term (Arndt et al., 2001). However, as water deficits increased, osmotic adjustment occurred concomitant with an increased root:shoot ratio to access deep soil moisture reserves, followed by leaf loss and ultimately drought-enforced dormancy (Arndt et al., 2001; Clifford et al., 1998).
This paper examines the location of mucilages in Z. rotundifolia and Z. mauritiana and studies the effects of drought-stress treatments imposed in two separate experiments on the changes in abundance and chemical composition of crude mucilage extracts. The ecophysiological implications of mucilages and associated polysaccharides in Ziziphus species are discussed.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResults and discussionConclusionReferences |
|---|
Localization of mucilages
Samples for anatomical studies were taken from the collection of Z. mauritiana (Gola) and Z. rotundifolia held in the glasshouse at HRI, Wellesbourne UK. Trees were grown in 65 l pots in a free-draining growing medium containing equal parts Levingtons C2, grit and John Innes No 2. Pre-sampling, the average day/night temperatures were 24/17 °C, with 2.14/1.45 kPa vapour pressure deficit and 370 µmol m-2 s-1 photosynthetically active radiation. Small (not >5 mm square) pieces were cut from the central leaf lamina and secondary stem. Material was either mounted in Tissue Tek O.C.TTM medium (Sakura bv, The Netherlands) and sectioned fresh using a cryo-microtome (Bright Instruments Ltd, Huntingdon, UK), or vacuum infiltrated for 3 h in 3% glutaraldehyde (0.1 M phosphate buffer pH 7.2), dehydrated through a graded ethanol series and embedded in London Resin White resin. Fresh sections were stained with 1% alcian blue for polyanionic polysaccharides (O'Brian and McCully, 1981
), whilst 1 µm resin sections were cut (Reichert-Jung Ultracut) and stained for light microscopy using azure/methylene blue (Richardson et al., 1960), periodic acid-Schiff (PAS) for starch and polysaccharides (Jensen, 1962), or toluidine blue-O, a general polyanionic stain (Feder and O'Brien, 1968).
Chemical analyses of mucilage
Changes in mucilage content during drought-stress
Foliar samples for mucilage analysis were derived from two separate studies investigating drought-stress: one using Z. mauritiana and the second using Z. rotundifolia. (1) Potted Z. mauritiana trees were exposed to a single 12 d drought-stress cycle as described previously (Clifford et al., 1998). (2) In the second experiment, 2-year-old potted Z. rotundifolia seedlings were exposed to either gradual or rapid drought-stress development imposed through regulated deficit irrigation over a 34 d cycle as described earlier (Arndt et al., 2001).
For chemical analyses, leaf material was collected from both treatments pre-stress and after 12 d in experiment (1), whilst in experiment (2), comparisons were made between control and both stress regimes after 34 d of treatment. In all treatments, foliar samples were collected and analysed from four trees per treatment.
Extraction and purification of water-soluble polysaccharides
Data on content and chemical composition of Ziziphus leaf mucilage were compared with that of commercially available (Flos Tiliae EAB, Vienna, Austria) lime tree flower mucilage (Tilia cordata L.) for which content and composition is well documented (Kram and Franz, 1983, 1985). Samples of Ziziphus and lime tree flower mucilage were analysed in parallel.
For Ziziphus, dried leaf samples were ground to a fine powder in a ball mill (Retsch MM2, Vienna, Austria). Water-soluble polysaccharides were extracted from 100 mg dried leaf material in 2 ml water at 20 °C. The extracts were shaken, put in an ultrasonic bath for 2 min, incubated for 15 min in a water bath at 35 °C and shaken for 2 h on a horizontal shaker. After centrifugation, the superanatant was removed and stored. The pellet was re-extracted twice more using the same procedure, and the aqueous supernatants combined prior to dialysis (MWCO 12–14 kDa, ZelluTrans, Roth, Karlsruhe, Germany) for 16 h, to remove all low molecular weight compounds. The dialysed extracts were freeze-dried and the dry weight of the lyophilized crude mucilage determined.
Enzymatic hydrolysis of polysaccharides and starch
Water-soluble polysaccharides extracted with the leaf mucilage were enzymatically degraded to glucose monomers using a combined -amylase and amyloglucosidase hydrolysis. Glucose was quantified by high performance anion exchange chromatography as described previously (Arndt et al., 2000).
Starch
After repeated extraction of low molecular weight carbohydrates of homogenized leaf samples with ethanol:water mixtures (Ho, 1976) and enzymatic degradation of starch with heat stable -amylase and amyloglucosidase, glucose was quantified by high performance anion exchange chromatography (HPAEC-PAD; DX 500 and ED 40, Dionex, Vienna, Austria (Arndt et al., 2000)).
Acidic hydrolysis of crude mucilage
Acid hydrolysis of the crude mucilage was performed by adding 300 µl 2 M trifluoroacetic acid to 1 mg of crude mucilage and incubating at 120 °C for 90 min. After centrifugation (5 min, 15000 rpm), the sample was dried under vacuum. Twice, the sample was redissolved in water and redried under vacuum to remove any remaining acid. Carbohydrates were determined using gas chromatography (Arndt et al., 2000).
Water relations
Pre-dawn leaf water status was determined for each treatment using a pressure chamber as described previously (Clifford et al., 1998), in eight trees per treatment in experiment 1 (3 outer canopy fully expanded leaves per tree), and in shoots from five trees per treatment in experiment 2.
From the second drought experiment described above, pressure–volume curves were derived for three trees in each of the control and gradual stress treatments (three replicate shoots per tree), both pre-stress, and after 34 d of treatment, with irrigated controls measured on each occasion. The repeat pressurization technique was used as described previously (Clifford et al., 1998). Water potential isotherms were constructed from the pressure–volume data.
Data analysis
Data for replicate trees were analysed by analysis of variance as a 2x2 factorial using Genstat 5 for Windows (version 4.1; Lawes Agricultural Trust, Rothamsted Experimental Station, UK).
|
Results and discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResults and discussionConclusionReferences |
|---|
Leaf anatomy and localization of mucilage
In Z. mauritiana, the abaxial leaf surface was characteristically densely pubescent, with numerous stomata arranged in the interveinal regions, whereas the adaxial surface was glabrous, with comparatively few, sunken stomata. Leaf hairiness, hypostomatous distribution and sunken stomata are all characteristic features of species that exist in drought-prone regions. Transverse sections from fresh leaf lamina material showed that both Ziziphus species have characteristic C3 anatomy, with an abundance of mucilaginous material exclusively localized in the adaxial epidermal cells which stained intensely with the mucopolysaccharide stain, alcian blue (Fig. 1a
). The mucilage-cell contents also stained positively and uniformly with the periodic acid-Schiff reagent (PAS), indicating a high polysaccharide content throughout the cell (rather than localized as would be seen in amyloplasts). When stained with the PAS/toluidine blue-O combination for light microscopy, there was no discernible nucleus, vacuole or cellular organelles in the epidermal mucilage cells, but with numerous starch grains and nuclei clearly visible in the mesophyll parenchyma (Fig. 1b) as previously reported for Salix (Mariani et al., 1988). Mucilage, produced in Golgi, accumulates initially between the plasmalemma and the cell wall, and after prolonged mucilage deposition, the remaining cytoplasm becomes compressed against the outer periclinal cell wall and degenerates (Bakker and Gerritsen, 1992). In contrast to the intracellular mucilage secretion observed in Ziziphus, in the high polysaccharide subspecies of Hemizonia luzifolia, leaves have been shown to have large volumes of extracellular mucilage within the spongy-mesophyll layer (Morse, 1990).
|
Although mucilages in the leaf lamina of Ziziphus were intracellular, the cortical and peripheral parenchyma of the major leaf veins and stems contained significant amounts of extracellular mucilage. The leaf veins had mucilage-filled spaces between the large-thin-walled outer collenchymatous cortical cells (Fig. 1c
), whilst in the stem, intercellular spaces in the central cortex and in the peripheral cortex surrounding the phloem were filled with mucilage (Fig. 1d) which, when viewed in longitudinal section, formed intercellular channels (Fig. 1e). A similar pattern of schizogenous mucilage has also been reported for Hibiscus schizopetalus, in which the degeneration of mature mucilage cells resulted in canal like, mucilage-filled cavities running parallel to minor veins (Bakker and Gerritsen, 1992).
Impact of drought-stress on leaf mucilage content
Data from both drought experiments showed that the total amount of mucilage was similar in both species with, on average, leaves of Z. mauritiana and Z. rotundifolia typically containing 7.1% and 9.6% mucilage, respectively, on a leaf dry matter (DM) basis (Table 1). Compared to most other species, and particularly tree species, these values are high and most of the species listed in Table 1 contained not more than 3% mucilage in their leaves (expressed on DM basis). In contrast to this are species that accumulate high levels of extracellular mucilage, such as the annual composite Hemizonia luzifolia (4–30% DM depending on subspecies (Morse, 1990)), and cacti up to 37% DM, (Nobel et al., 1992).
|
In neither experiment was the total amount of mucilage in the leaves of Ziziphus affected by drought (Table 2
). This is similar to the report that there were no differences in the water-soluble mucilage content extracted from Boraginaceae from wet and dry habitats (Pollak and Albert, 1990), but contrasts with early findings in Prunella (Volk, 1938), Brunella grandifolia (Jeremias, 1966) in which mucilaginous substances increased during drought-stress. Seasonal variation in leaf mucilage content was reported (Diestelbarth and Kull, 1985) and it is possible that, either the duration of stress in the current studies may have been too short (12 d and 34 d) to affect gross mucilage metabolism, or that any underlying decrease in mucilage may have been offset by the accumulation of another unidentified polymer.
|
Mucilage composition
Acid hydrolysis of crude leaf mucilage extract in both Z. mauritiana and Z. rotundifolia revealed that the main sugar constituents were rhamnose, glucose, galactose, and arabinose (Table 1). The most interesting observation was the extremely high glucose content in the crude mucilage extracts for both Ziziphus species, with at least 2-fold higher glucose content compared with other species for which data are available (Table 1). The hexuronic acids, galacturonic acid and glucuronic acid, were also present in the hydrolysate, but at lower concentrations than the main sugar components (data not shown), and the high levels of the neutral sugars rhamnose, galactose and arabinose are consistent with published leaf mucilage composition for other species (Table 1). Leaf mucilages usually have pectin like structures with large amounts of D-galactose and L-arabinose (Bräutigam and Franz, 1985b), with the disaccharide 4--galacturonosylgalacturonic acid as the major repeating unit (Bailey, 1965). However, mucilages generally comprise a mixture of polysaccharides (Bräutigam and Franz, 1985a; Müller et al., 1989) and the high glucose levels resulting from the acid hydrolysis of the water-soluble mucilage extract in Ziziphus may suggest the presence of abundant glycosidic polysaccharides, or glucans. To test this idea, crude leaf mucilage extract from Ziziphus was enzymatically hydrolysed with -amylase and amyloglucosidase, and compared with the well-characterized mucilage from lime tree (Tilia) flowers (Table 1). Alpha-amylase and amyloglucosidase are two specific enzymes that hydrolyse -1,4 and -1,6 glycosidic linkages and are commonly used in starch determination to degrade the two major starch constituents amylose and amylopectin. Compared to Tilia flower mucilage, relatively high glucose concentrations were measured following enzymatic degradation of Ziziphus mucilage extracts. It is extremely unlikely that the glucose was starch-derived, since foliar starch would be insoluble in water at 30 °C, the extraction temperature for mucilages in the current study, which was well below the gelatinization point (Morrison, 1992). Alpha-amylase and amyloglucosidase do not possess the mixed linked ß-glucanase activity necessary to hydrolyse ß-glycosidic bondages (Åman and Hesselman, 1984), and therefore it is also unlikely that glucose was released directly from a mucilaginous polysaccharide, since glycosides, which contain uronic acid, are commonly linked in ß-glycosidic bonds (Bailey, 1965) as has been demonstrated for leaf mucilage from Plantago lanceolata (Bräutigam and Franz, 1985b). Consequently, the most likely source of the glucose would be a water-soluble glucan, present at high concentrations in Ziziphus leaves, that was co-extracted with the mucilage, as has been reported previously for Tilia flower mucilage, in which it was also suggested that the glucose was glucan- rather than starch-derived (Kram and Franz, 1983).
Data from enzymatic hydrolysis also revealed that in both Ziziphus species, the glucose content in crude mucilage declined significantly during drought-stress (Table 2), and that the extent of the decrease was associated with the degree of drought-stress, with significantly lower glucose contents in rapidly- than in gradually-stressed leaves at the end of the 34 d drought cycle. The large reductions in glucose content indicates that the foliar glucan may be relatively easily metabolized or remobilized. However, from the available data, it is not possible to localize the glucan within the leaf tissue. However, if one assumes that the majority of mucilage cells are metabolically inactive (see above), the observed decrease in glucose during drought-stress indicates that the glucan may be located in the metabolically active mesophyll or epidermal cells. In addition, it is conceivable that water-soluble glucans occur more frequently also in other plant species, but that they have not been detected due to the conventional procedures used for starch analysis. During starch determination in plant samples low molecular weight compounds are removed by repeated washing of ground plant material with ethanolic solutions. Therefore, any water-soluble glucans, which are not soluble in ethanol, are degraded with starch in the subsequent enzymatic hydrolysis and consequently, their presence may result in erroneous starch determination.
Previous studies showed that during drought-stress, starch levels declined, with large increases in the concentrations of hexose sugars in the crude bulk leaf extract. The current work indicates that although stored starch may contribute to increases in hexoses during drought-stress, a high proportion of solute accumulation in bulk leaf tissue may be accounted for by the high levels (1–2% DM, derived from Table 2) of water-soluble glucan extracted together with the mucilage. This would provide a source of easily degradable carbohydrate contributing to rapid remobilization of sugars and solutes for osmotic adjustment, cyclitol and proline accumulation (Clifford et al., 1998), and increased root:shoot ratio (Arndt et al., 2000) observed in Ziziphus during drought-stress.
Effects of drought-stress on relative leaf capacitance
Data in Fig. 2 superimpose the water potential isotherms (changes in 
leaf with relative water content (
)) from both experiments for bulk leaf tissue of control irrigated and drought-stressed Z. rotundifolia and Z. mauritiana. For each irrigation treatment, concomitant with the similar amounts of mucilage in both species, the water potential isotherms were very similar. In Z. mauritiana, changed more quickly per unit change in leaf over the first 5% drop in than in Z. rotundifolia, but was similar thereafter. This shows that, under irrigated conditions, Z. rotundifolia may generate a slightly more negative in the plant, thereby improving water uptake under these conditions for favourable growth in this vigorous species. Indeed, this may be one reason why Z. rotundifolia has commonly been used as a rootstock for selectively improved, large-fruited (less vigorous) cultivars of Ziziphus in India.
|
Comparing the isotherms from the different irrigation treatments, below
of 
92%, leaf in the drought-stressed treatments continued to decline more rapidly per unit change in than in the irrigated controls (Fig. 2). This is consistent with the accumulation of solutes in the bulk leaf tissue and osmotic adjustment as reported previously for both species (Clifford et al., 1998; Arndt et al., 2001), with a higher maintained for a given value of leaf. From the pressure–volume curves, it was clear that although leaf was depressed during drought-stress, the point of turgor loss was the same in droughted and irrigated controls (Clifford et al., 1998). This was due to a decrease in cell wall elasticity as drought developed and may be a short-term adaptation both to improve the ability of the plant to extract moisture from a progressively drying soil profile, and to maintain cell volume and metabolic activity at low soil water potential.
Due to the colloidal nature of mucopolysacchardes, their capacitance is generally high (Goldstein and Nobel, 1991), so they can lose significant amounts of water without large changes in water potential (Morse, 1990). In comparison with other species in which mucilages are reported to play an important role in plant water relations, the relative capacitance of leaves in Ziziphus is no greater than 0.21 MPa-1 (Fig. 2), which lies towards the lower end of the range reported for the high and low polysaccharide subspecies of Hemizonia luzifolia: 0.7 MPa-1 and 0.08 MPa-1, respectively. In cacti, relative capacitance of the cladode parenchyma is 1.04 MPa-1, with large amounts of mucilage-associated solutes which may aid their function as an apoplastic capacitor (Nobel et al., 1992). The most important difference between Ziziphus and these genera is that Hemizonia and cacti characteristically have large amounts of extracellular mucilage, whereas Ziziphus appears to have predominantly intracellular mucilage in the leaf lamina adjacent to the mesophyll cells. These observations confirm the idea that extracellular mucilages are effective in affecting cell water relations and increasing capacitance, with intracellular mucilages, as observed in Ziziphus, making no contribution to cellular capacitance (Morse, 1990).
As drought-stress intensified, leaf loss ensued, with an 80% reduction in leaf area by the end of the drying cycle in the rapid stress treatment (Arndt et al., 2001). Following the trial, the stressed trees were irrigated after 2 months without water. There was a rapid regrowth of shoots with recovery of the canopy (unpublished data).
In multi-site field trials of Ziziphus in Zimbabwe, trees grown in the Highveld areas subjected to sub-zero temperatures suffered high levels of foliar damage and loss, indicating that the foliar mucilage was ineffective in conferring low temperature tolerance. One potential role for foliar mucilages in Ziziphus may be as a store of secondary metabolites to deter herbivory or pathogens (Davis et al., 1986), but from the current study, there are no data available to test this. Therefore mucilages do not appear to benefit plant water relations in transpiring tissues, and following drought-enforced leaf loss, remobilization of solutes from water-soluble glucans and starch in the stems and roots (Arndt et al., 2001), act as significant carbohydrate and solute sources for survival during prolonged drought, facilitating rapid regeneration of shoot material once conditions become more favourable.
|
Conclusion |
|---|
|
TopAbstractIntroductionMaterials and methodsResults and discussionConclusionReferences |
|---|
Large amounts of intracellular mucilage were present in the leaf lamina of Ziziphus, with extracellular mucilages in the main leaf veins and stem cortex. Data from the two drought experiments showed that there were no changes in total mucilage content during drought-stress, and that the predominantly intracellular foliar mucilages were ineffective in altering leaf capacitance during drought-stress, with water relations being dominated by changes in solute concentration and decreasing wall elasticity.
Biochemical analysis of the water-soluble polysaccharides, extracted together with the mucilage using enzymatic hydrolysis, indicated that a water-soluble glucan may be present in the mucilage extract. The main role of the glucan, together with foliar starch, may be as significant sources of monosaccharide sugars contributing to osmotic adjustment in the short-term, and to remobilization of solutes to other sink organs as drought intensified. By providing a form of energy and solute storage in non-transpiring tissue, glucans may together with starch, support survival during dry periods and promote rapid regrowth following rainfall.
|
Acknowledgments |
|---|
We acknowledge the European Commission, MAFF and BBSRC for funding the research (contract TS3*-CT93-0222) and Dr Wolfgang Wanek, John Andrews and Andrew Mead for their useful and constructive comments.
|
Notes |
|---|
5 To whom correspondence should be addressed. Fax: +44 1789 470552. E-mail: sean.clifford{at}hri.ac.uk
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResults and discussionConclusionReferences |
|---|
Åman P, Hesselman K. 1984. Analysis of starch and other main constituents of cereal grains. Swedisch Journal of Agricultural Research 14, 135–139.
Arndt SK, Clifford SC, Wanek W, Jones HG, Popp M. 2001. Physiological and morphological adaptations of the fruit tree Ziziphus rotundifolia in response to progressive drought-stress. Tree Physiology 21, 705–715.[Abstract]
Arndt SK, Wanek W, Clifford SC, Popp M. 2000. Contrasting adaptations to drought-stress in field-grown Ziziphus mauritiana and Prunus persica trees: water relations, osmotic adjustment and carbon isotope composition. Australian Journal of Plant Physiology 27, 985–996.[Web of Science]
Bailey RW. 1965. Oligosaccharides. Oxford: Pergamon Press.
Bakker ME, Gerritsen AF. 1992. The development of mucilage cells in Hibiscus schizopetalus. Acta Botanica Neerlandica 41, 31–42.[Web of Science]
Benhura MAN, Marume M. 1993. The mucilaginous polysaccharide material isolated from ruredzo (Dicerocaryum zanguebarium). Food Chemistry 46, 7–11.
Bräutigam M, Franz G. 1985a. Schleimpolysaccharide aus Spitzwegerichblättern. Deutsche Apotheker Zeitung 125, 58–62.
Bräutigam M, Franz G. 1985b. Structural features of Plantago lanceolata mucilage. Planta Medica 4, 293–297.
Clarke AE, Andreson RL, Stone BA. 1979. Form and function of arabinogalactans and arabinogalactan-proteins. Phytochemistry 18, 521–540.[Web of Science]
Clifford SC, Arndt SK, Corlett JE, Joshi S, Sankhla N, Popp M, Jones HG. 1998. The role of solute accumulation, osmotic adjustment and changes in cell wall elasticity in drought tolerance in Ziziphus mauritiana Lamk. Journal of Experimental Botany 49, 967–977.
Clifford SC, Kadzere I, Jones HG, Jackson JE. 1997. Field comparisons of photosynthesis and leaf conductance in Ziziphus mauritiana and other fruit tree species in Zimbabwe. Trees 11, 449–454.
Davis KR, Darvill AG, Albersheim P, Dell A. 1986. Host–pathogen interactions. XXIX. Oligogalacturonides released from sodium polypectate by endopolygalacturonic acid lyase are elicitors of phytoalexines in soybean. Plant Physiology 80, 568–577.
Diestelbarth H, Kull U. 1985. Physiological investigations of leaf mucilages. II. The mucilages of Taxus baccata L. and of Thuja occidentalis L. Israel Journal of Botany 34, 113–128.[Web of Science]
Feder N, O'Brien MS. 1968. Plant microtechnique: some principles and new methods. American Journal of Botany 55, 123–142.[Web of Science]
Franz G. 1966. Die Schleimpolysaccharide von Althena officinalis und Malva sylvestris. Planta Medica 14, 89–110.
Franz G. 1979. Metabolism of reserve polysaccharides in tubers of Orchis morio L. Planta Medica 36, 68–73.[Web of Science][Medline]
Franz G. 1989. Polysaccharides in pharmacy: current applications and future concepts. Planta Medica 55, 493–497.[Medline]
Goldstein G, Nobel PS. 1991. Changes in osmotic pressure and mucilage during low-temperature acclimation of Opuntia ficus-indica. Plant Physiology 97, 954–961.
Hegnauer R. 1973. Chemotaxonomie der Pflanzen, Band 6: Dicotyledoneae: Rafflesiaceae–Zygophyllaceae. Basel und Stuttgart: Birkhäuser Verlag.
Ho LC. 1976. The relationship between the rates of carbon transport and photosynthesis in tomato leaves. Journal of Experimental Botany 27, 87–97.
Höllriegl H, Koehler H, Franz G. 1986. Über höhermolekulare Polysaccharide aus den Blättern von Ginko biloba. Scientia Pharmaceutica 54, 321–330.
Jawanda JS, Bal JS. 1978. The ber, highly paying and rich in food value. Indian Horticulture Oct–Dec,19–21.
Jensen WA. 1962. Botanical histochemistry. WH Freeman and Co.: San Francisco.
Jeremias K. 1966. Der Einfluß der Bodentrockenheit auf den Zuckergehalt vegetativer Pflanzenteile. Zeitschrift für Pflanzenphysiologie 54, 237–239.
Kram G, Franz G. 1983. Untersuchungen über die Schleimpolysaccharide aus Lindenblüten. Planta Medica 49, 149–153.[Web of Science][Medline]
Kram G, Franz G. 1985. Structural investigations on watersoluble polysaccharides of lime tree flowers (Tilia cordata L.). Pharmazie 40, 501–502.[Web of Science]
Lipp CC, Goldstein G, Meinzer FC, Niemczura W. 1994. Freezing tolerance and avoidance in high-elevation Hawaiian plants. Plant, Cell and Environment 17, 1035–1044.
Mariani P, Rascio N, Baldan B, Paiero P, Urso T. 1988. Epidermal mucilage cells in leaves of Salix species. Flora 181, 137–145.[Web of Science]
Metcalf CR, Chalk L. 1950. Anatomy of the Dicotyledons, Vol. 1. Oxford: Claredon Press.
Morrison WR. 1992. Analysis of cereal starches. In: Linskens HF, Jackson JF, eds. Seed analysis. Berlin: Springer Verlag.
Morse SR. 1990. Water balance in Hemizonia luzulifolia: the role of extracellular polysaccharides. Plant, Cell and Environment 13, 39–48.
Müller BM, Kraus J, Franz G. 1989. Chemical structure and biological activity of water soluble polysaccharides from Cassia angustifolia leaves. Planta Medica 55, 536–539.[Medline]
Naglschmid F, Kull U, Jeremias K. 1982. Physiologische Untersuchungen über Blattschleime. 1. Untersuchungen an Verbascum densiflorum. Biochemie und Physiologie der Pflanzen 177, 671–685.[Web of Science]
Nobel PS, Cavelier J, Andrade JL. 1992. Mucilage in cacti: its apoplastic capacitance, associated solutes and influence on tissue water relations. Journal of Experimental Botany 43, 641–648.
O'Brian TP, McCully ME. 1981. The study of plant structure: principles and selected methods. Australia: Termarcarphi Pty Ltd.
Pimienta-Barrios E, Nobel PS. 1998. Vegetative, reproductive, and physiological adaptations to aridity of pitayo (Stenocereus queretaroensis, Cactaceae). Economic Botany 52, 401–411.
Pollak J, Albert R. 1990. Stoffwechselphysiologische Charakterisierung der Boraginaceen unter besonderer Berücksichtigung ökologischer Aspekte. Flora 184, 151–168.[Web of Science]
Richardson KC, Jarett L, Finke EH. 1960. Embedding in epoxy resin for ultrathin sectioning in electron microscopy. Stain Technology 35, 313–323.[Web of Science][Medline]
Robichaux RH, Morse SR. 1990. Extracellular polysaccharide and leaf capacitance in a hawaian bog species, Argyroxiphum grayanum (Compositae-Madiinae). American Journal of Botany 77, 134–138.[Web of Science]
Tomoda M, Gonda R, Shimizu N, Yamada H. 1989. Plant mucilages. XLII. An anti-complementary mucilage from the leaves of Malva sylvestris var. mauritiana. Chemical and Pharmaceutical Bulletin 37, 3029–3032.
Trachtenberg S, Mayer AM. 1981. Composition and properties of Opuntia ficus-indica mucilage. Phytochemistry 20, 2665–2668.[Web of Science]
Trachtenberg S, Mayer AM. 1982. Biophysical properties of Opuntia ficus-indica mucilage. Phytochemistry 21, 2835–2843.[Web of Science]
Volk OH. 1938. Untersuchungen über das Verhalten der osmotischen Werte von Pflanzen. Zeitschrift für Botanik 32, 65–149.
Zimmermann U, Zhu JJ, Meinzer FC, Goldstein G, Schneider H, Zimmermann G, Benkert R, Thürmer F, Melcher P, Webb D, Haase A. 1994. High molecular weight organic compounds in the xylem sap of mangroves: implications for long-distance water-transport. Botanica Acta 107, 218–229.[Web of Science]
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||