Journal of Experimental Botany, Vol. 51, No. 344, pp. 595-603,
March 2000
© 2000 Oxford University Press
Cell wall adaptations to multiple environmental stresses in maize roots
Julius-von-Sachs-Institut für Biowissenschaften, Lehrstuhl Botanik I, Universität Würzburg, Germany
Received 19 July 1999; Accepted 10 October 1999
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
A municipal solid-waste bottom slag was used to grow maize plants under various abiotic stresses (high pH, high salt and high heavy metal content) and to analyse the structural and chemical adaptations of the cell walls of various root tissues. When compared with roots of control plants, more intensive wall thickenings were detected in the inner tangential wall of the endodermis. In addition, phi thickenings in the rhizodermis in the oldest part of the seminal root were induced when plants were grown in the slag. The role of the phi thickenings may not be a barrier for solutes as an apoplastic dye could freely diffuse through them. The chemical composition of cell walls from endodermis and hypodermis was analysed. Slag-grown plants had higher amounts of lignin in endodermal cell walls when compared to control plants and a higher proportion of H-type lignin in the cell walls of the hypodermis. Finally, the amount of aliphatic suberin in both endo- and hypodermal cell walls was not affected by growing the plants on slag. The role of these changes in relation to the increase in mechanical strengthening of the root is discussed.
Key words: Endodermis, exodermis, heavy metals, lignin, phi thickenings.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Plants have developed a variety of strategies and mechanisms to react to any change of their environment. Anatomical and physiological adaptations allow better growth under unfavourable conditions. The root system is particularly affected by these changes because the root is that part of the plant which is in direct contact to the contaminated soil substrate. A number of studies have shown the alterations of root architecture and structure induced by a variety of stressful conditions (Neumann et al., 1994
; Shannon et al., 1994; Tsegaye and Mullins, 1994; Plaut et al., 1997). For instance, it is known that plants respond to salt stress by a reduction in root growth and length. A decrease in the diameter of wheat roots and of the transectional area of cortical cells was observed with heavy metal treatment (Setia and Bala, 1994).
Besides changes in external root morphology there are also alterations in the fine structure of the root. It has been shown (Shannon et al., 1994) that salinity promotes suberization of the hypodermis and endodermis and that the Casparian strip is developed closer to the root tip than in non saline roots. In cotton seedling roots, the formation of an exodermis can be induced by salinity (Reinhardt and Rost, 1995). In addition, some plant species develop cell wall thickenings in different root tissues. These thickenings are modifications of the mid-portion of the radial cell walls and are therefore called phi thickenings. They can either form a uniseriate or a multiseriate layer (Guttenberg, 1968; Peterson et al., 1981; Eschrich, 1995). Phi thickenings are formed on the walls of certain cell layers in the root cortex of several species of gymnosperms (Taxaceae, Podocarpaceae, Cupressaceae) (Guttenberg, 1968; Haas et al., 1976) and a few families of angiosperms (Rosaceae, Geraniaceae, Berberidaceae, Sapindaceae) (Peterson et al., 1981; Praktikakis et al., 1998). Thickenings can also be formed in the hypodermis (e.g. geranium, Haas et al., 1976). All species reported in the literature are dicotyledons. However, the occurrence of phi thickenings in roots of monocotyledons has not yet been documented.
Bulk density, porosity and mechanical impedance are other factors influencing root growth and extension (Bennie, 1996). Increased mechanical impedance slows root extension and can alter cell size and cell number in the cortex (Goss and Russell, 1980).
In this study, two different soil substrates were compared for their effect on the growth of corn roots: garden mould was used as a control substrate and MSW (municipal solid waste) bottom incinerator slag was used as a contaminated substrate including different sources of stress like salinity, high pH, heavy metals, and high mechanical impedance. MSW incinerator slag is used in Germany in accordance with German law as support and construction material (LAGA, 1994). In general, it is used for roads, banks or parking lots as a 30–50 cm thick top layer. The environmental compatibility of this application is under discussion.
The aim of this study was to investigate how tissues in corn roots were affected by the presence of various sources of stress. Therefore, not only the development and structure of the root, but also particular components of the cell wall were examined.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Plant material
Seeds of corn (Zea mays L. cv. Garant FAO 240) were obtained from Asgrow GmbH, Bruchsal, Germany. Seeds were imbibed in aerated water overnight and planted in pots (90 mm diameter) filled with soil. Plants were grown in a greenhouse (20 °C, 16/8 h, light/dark) for 20 d, and watered daily with tap water.
Soil substrates
Processed MSW slag, obtained from a MSW slag processing plant Würzburg (CC Reststoff GmbH, Germany), was used as a substrate expected to induce various kinds of stresses (alkaline and salt stress, heavy metal stress) on plant roots.
In order to distinguish the alkaline stress from the salt stress of the slag, the salt burden of the slag was removed by washing with a 3-fold volume of water. For this purpose a defined volume of slag was put into an Erlenmeyer flask, the same volume of distilled water was added and the mixture was shaken for 1 h. Then the mixture was allowed to settle, filtered and the solid was resuspended with fresh water. This procedure was repeated three times. The supernatant was discarded, the slag was dried at 105 °C and stored until use.
A garden mould composed of organic soil, peat and sand in a ratio of 4 : 2:1, by vol. was used as a reference soil. Before use the organic soil was steam-heated (20 min, 90 °C) to kill fungi and weed seeds.
Element analysis
The elemental composition of the municipal incinerator slag and the garden mould was determined after homogenization of samples and pressurized extraction in ultra grade 65% HNO3 (170 °C, 10 h) by ICP emission spectroscopy (ICP Jobin 70 plus, ISA GmbH, Grasbrunn, Germany).
Soil physical properties
Mechanical impedance was determined by a penetrometer (Ele, Great Britain). For determination of the bulk density (mass of dried soil per unit volume) the soil substrates were dried at 105 °C, placed in a calibrated glass cylinder and weighed.
Soil solution
Soil solutions were obtained by negative pressure filtration with suction cups (ceramics suction cups, Oekos, Göttingen, Germany).
Microscopic techniques
For all microscopic investigations sections were made in the upper third of the primary roots. By reason of different root growth of slag and control plants, the whole root was divided into three parts. For slag roots, the upper third is 1–5 cm from the root base, for control roots 1–15 cm. Before use, root segments were fixed for 24 h in a phosphate buffer (10 mM, pH 7.4) containing 3.7% (w/w) formaldehyde. Sections of 20 µm were cut at -25 °C using a cryomicrotome (Cryostat H 500 M; Microm) and examined by an Axioplan microscope (Zeiss, Oberkochen, Germany) equipped with an Osram HBO 50 W mercury lamp and Zeiss filter sets (exciter filter 365 nm, dichroitic mirror FT 395, barrier filter LP 395).
Tracer application
To test the permeability properties of the phi thickenings, a berberine–thiocyanate tracer procedure was applied (Enstone and Peterson, 1992). The chemicals necessary for the experiment were obtained from Sigma (Deisenhofen, Germany). The movement of the fluorescent dye was observed on sections under blue light using an axioplan microscope (Carl Zeiss, Oberkochen, Germany).
The Casparian bands of endodermis and hypodermis were visualized by treating root sections with 0.1% berberine hemisulphate for 1 h, rinsing the tissue several times with water and transferring to a 0.5% toluidine blue staining solution for 30 min. Toluidine blue is used instead of aniline blue. The tissue was rinsed once again with distilled water, then placed on slides in mounting medium (0.1% FeCl3 in 50% glycerol) and viewed under violet fluorescence excitation (Brundrett et al., 1988).
Isolation of hypodermal and endodermal cell walls
The isolation and purification procedures of cell walls of the hypodermis and endodermis have been described in detail previously (Schreiber et al., 1994). Roots were cut into segments of approximately 5 cm length using a razor blade. Root segments were incubated at room temperature in a citric buffer solution (10-2 M, pH 3) containing cellulase (Onozuka R-10, Serva, Heidelberg) and pectinase (Macerozyme R-10, Serva, Heidelberg). Sodium azide was added to prevent microbial growth. After 10–15 d of enzymatic digestion, hypodermal and endodermal cell walls were separated by means of two forceps and a binocular microscope (SZ 30, Olympus, Hamburg).
Determination of lignin and suberin
Thioacidolysis:
To detect the biopolymer lignin, isolated cell wall material was subjected to the thioacidolysis-procedure (according to Lapierre et al., 1991). Cell wall isolates were stirred in a mixture of BF3 etherate (Merck, Darmstadt, Germany), ethanethiol (Fluka, Neu-Ulm) and dioxane in argon atmosphere at 100 °C for 4 h. The reaction mixture was allowed to cool, diluted with 2 ml water and extracted three times with 3 ml of CHCl3 containing 20 µg dotriacontane (Fluka) as internal standard. The combined organic phases were dried with Na2SO4.
Transesterification:
The degradation of cell wall material for detecting suberin was carried out according to the transesterification method (Kolattukudy and Agrawal, 1974). 0.5–1 mg of isolated cell wall material was added to 1 ml of a 10% BF3/methanol solution (Fluka). The reaction mixture was heated to 70 °C for 24 h. After cooling, the solution was removed from the cell wall sample and collected. The cell walls were washed three times with 1 ml CHCl3 containing 20 µg dotriacontane (Fluka) as internal standard. The chloroformic and methanolic solutions were combined and washed twice with 2 ml saturated sodium chloride solution. The organic phase was separated and dried with Na2SO4.
Gas chromatography and mass spectrometry
Gas chromatographic analysis and mass spectrometric identification of the reaction products obtained by thioacidolysis and transesterification were performed as described in detail previously (Zeier and Schreiber, 1997). Separation and quantitative sample analysis were achieved by a gas chromatograph (HP 5890 Series II gas chromatograph, Hewlett-Packard, California, USA) equipped with a flame ionization detector. Qualitative sample analysis was carried out on a gas chromatograph (HP 5890 Series II gas chromatograph, Hewlett-Packard) coupled with a quadrupole mass selective detector (HP 5971 mass selective detector, Hewlett-Packard). Before injecting, samples were derivatized using BSTFA (N,N-bis-trimethylsilyl-trifluoroacetamide, Machery-Nagel, Düren).
Analysis of amino acids
Cell wall isolates were hydrolysed with 1 ml 6 N HCl (130 °C, 24 h, argon atmosphere). After filtration the hydrochloric acid was removed (20 mbar, 40 °C), the residue washed twice with 1 ml distilled water and the aquatic solvent was evaporated again. Then 200 µl sample buffer (0.1 M lithium citrate, 68.5 mM citric acid, 20 mM bis-(2-hydroxy-ethyl)-sulphide, pH 2.2) was added. Amino acids were analysed by HPLC (LC 5001 Biotronic, Eppendorf, Hamburg).
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Characterization of the soil substrates
MSW bottom slag compared to garden mould was characterized by its high Ca, Fe, Na, Cl, S, and B content (Table 1
), its high amount of heavy metals (Table 2) and its low N content (Table 1). When compared to garden mould the metals were 25–200-fold enriched (copper (60–180-fold), cadmium (50-fold), lead (25–50-fold), and zinc (25–50-fold)). A closer estimation of the phytotoxicity of this substrate is to assay the availability of these elements in the soil solution. In Table 3 the chemical composition of soil solutions obtained by suction cups is shown. The solutions exhibited strong alkaline pH values for slag and washed slag while the pH of the soil solution of garden mould was only slightly alkaline. Even though the amount of P and Fe was high in slag, these elements were hardly detectable in the soil solution, due to the insolubility of phosphate and iron compounds at alkaline pH. Furthermore, the electric conductivity of the slag soil solution indicated a 10 times higher concentration of solutes than in the reference soil solution. The main difference between slag and washed slag was the lower content of soluble salts (alkali-chloride and -sulphate) in washed slag. Details about the chemical composition of the soil solution of slag and other properties of MSW slag are listed (Fuchs et al., 1997). MSW slag is a rather inhomogeneous substrate (large differences in size of soil particles, 40% of slag particles are larger than 7 mm in comparison to 15% of the control soil). For a description of a soil substrate some physical properties should be mentioned as well. Compared to garden mould (0.07 MPa) the mechanical impedance of slag is increased about a factor of three (0.2 MPa). Bulk soil density of slag (1.14 g cm-3) was higher than that of garden mould (0.92 g cm3).
|
|
|
Modifications in root architecture and structure
The effect of culture in slag was first a reduction of root growth. Root length was reduced by 50% by cultivation on slag compared to garden mould (Table 4). However, the root : shoot ratio was increased for slag plants by a factor of 2. Root diameter was also affected. Roots grown in MSW slag were 14% thicker. Microscopic examination revealed that the increase of the root diameter was due to an increased thickness of the cortex (Table 4).
|
In roots of slag-grown plants intensive U-shaped thickenings of the inner tangential wall of the endodermis (Fig. 1A
) were observed. In the tertiary state of development endodermal cells deposit lignified cell wall material onto the suberin lamella. These deposits were pronounced more intensive in slag-cultivated roots (0.5±0.08 µm) than in control roots (0.32±0.04 µm) (Fig. 1B). Another phenomenon detected during the slag-cultivation of corn were cell wall modifications like phi thickenings in the radial cell walls of the rhizodermis (Fig. 1C, D). These phi thickenings were present only on slag culture. The development of phi thickenings during these experimental conditions was variable, both longitudinal and tangential. Thickenings were not formed continuously from the tip to the base, but occurred only in the upper third, the oldest part of the root. In addition, if present, phi thickenings did not occur continuously in the rhizodermal periphery of the root. Rather intermissions in thickening formation were observed. Between 6 and 50 adjacent rhizodermal cells formed clusters equipped with phi thickenings. Attempts to induce phi thickenings by treating roots with 100–200 mM NaCl in hydroponic culture or with sand as carrier material or by growing them in glass ballotini of varying size to simulate mechanical impedance failed (not shown). Also hydroponic and aeroponic cultures of Zea mays did not induce phi thickenings in the rhizodermis (Freundl et al., 2000).
|
To get more information about the importance of cell wall thickenings, the permeability properties were tested by application the apoplastic tracer berberine hemisulphate (Enstone and Peterson, 1992
). Berberine moves radially into the root and forms crystals with potassium thiocyanate. As shown in Fig. 1E the phi thickenings were penetrated, but the inward movement of the dye was stopped at the exodermis. The cell walls with phi thickenings were permeable for the apoplastic dye in contrast to the exodermal Casparian band. Figure 1F illustrates the occurrence of the Casparian band in the exodermis and endodermis and reveals that maize is an exodermal species (Enstone and Peterson, 1992).
Chemical composition of cell wall isolates
Lignin:
Quantitative chromatographic results revealed that isolated cell walls of the endodermal layer of slag-cultivated plants contained higher amounts of lignin than cell walls of control roots (Table 5). By contrast, roots grown in prewashed slag did not contain higher concentrations of lignin. Furthermore, variations in the lignin components were studied. The biopolymer lignin is composed of the cinnamic acid derivates p-coumaryl, coniferyl and sinapyl alcohols, which differ in the extent of methoxylation. According to the aromatic nucleus in the polymer the terms guaiacyl (G), syringyl (S) and p-hydroxyphenyl (H) are used. The monomeric composition of lignin showed a difference both between cell walls of the endodermis and hypodermis and between the cell wall material at different culture conditions. Although there was no effect of the growth substrate on the total lignin content of hypodermal cell walls (Table 5) there were variations in the proportions of the monomeric units of lignin. The proportion of the H-monomer in hypodermal cell walls was much higher than in endodermal tissue (Fig. 2A, B). Furthermore, growth on slag induced a higher proportion of H-units in hypodermal cell walls than in the control ones. In addition, hydroponically grown maize showed proportions of H-units even lower than garden mould (Fig. 2A). In endodermal cell walls the proportion of G-units were increased and the proportion of the S-units were decreased by growth on slag. G-units were the abundant monomer in the endodermis. In the hypodermis the proportion of the three monomers is more homogeneous.
|
|
Amino acids:
Hypodermal cell walls in roots of slag-treated maize plants exhibited a nearly 3-fold higher amount of p-hydroxyproline than the roots of the control plants (Table 6). The amount of the amino acids threonine, proline and histidine were also increased in roots of slag-cultivated maize plants. Finally, the sum of all detected amino acids in hypodermal cell wall material of slag-cultivated roots was higher than in control roots.
|
Hydrophobic compounds:
There was a significant higher amount of suberin in the cell wall of the hypodermis than in that of the endodermis (Fig. 3). However, there was no significant increase in the total amount of hypodermal suberin when the plants were grown on slag. It was also tested, whether growth of corn on slag would alter the composition of the suberin fraction. Figure 4 demonstrates that this was not the case. The proportion of 
-hydroxyacids (C16–C30), dicarboxylic acids (C16–C26), carboxcylic acids (C16–C26), alcohols (C16–C24), and 2-hydroxyacids (C16–C26) were roughly similar in hypodermis and endodermis and within a given cell wall type between the various treatments.
|
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Soil substrates
When MSW slag is used as soil substrate, plants experience various stresses: salinity, nutrient deficiency, heavy metal toxicity, alkaline pH, and compaction. High amounts of soluble salts, mainly alkali chloride and -sulphate salts are expected to cause considerable salt stress to plants (up to -0.5 MPa) while the low N content induces nitrogen deficiency. The low nitrogen content of slag is due to its origin by burning of waste at 800–1000 °C. The main difference between crude slag and prewashed slag is the amount of salt. When slag is washed with a 3-fold volume of water, most of the salt burden is removed because of the high solubility of alkali salts, mainly chlorides and sulphates.
The high pH of the soil solution of slag, which causes alkaline stress, produces additional nutrition deficiency. Although the elements P and Fe were present in higher concentration in slag than in garden mould, at alkaline pH they are scarcely available to the plant. Another stress arises from the heavy metal content. Even though the amount of heavy metals in slag is very high, the availability for plants is reduced due to the alkaline pH and the chemical binding form of the metals (sequential extraction procedure according to Tessier et al., 1979; not shown). Thus, the contribution of heavy metals to the total stress on slag-grown roots may be low.
Furthermore, plant growth was influenced by the compaction of the soil. Slag exhibits a stronger mechanical impedance for the root system to penetrate into the soil than the control substrate. It was reported that the extension rate of the root was reduced when an external pressure of about 100 kPa was applied (Goss and Russell, 1980). Other authors published values about 1.5 MPa as moderate impedance. However, a lower impedance may also impede root growth when soil aeration is low (Vepraskas, 1994). Typical bulk soil density of heavily compacted soils is about 1.5 g cm-3 (Iijima and Kono, 1992). Comparing with these data from literature the mechanical impedance of MSW slag could be valued as rather moderate and not severe.
Root structure
By cultivation of corn in slag, various architectural and structural changes were observed. The decrease in root length and the increase in root diameter are typical morphological changes for mechanically impeded roots (Bennie, 1996). Morphological and anatomical changes of roots of young maize were also observed when the seedlings had to penetrate soil of high mechanical impedance (Hartung et al., 1994). Salinity stress also causes a thickening of the root. The increased root to shoot ratio corresponds to the fact, that plants invest more energy in root than in shoot growth in order to increase absorption of ions when they suffer nutrient deficiency, here N and P.
Even though Zea mays is an intensively studied material, nothing else has been reported in the literature about the presence of cell wall modifications like phi thickenings in this plant to date. However, phi thickenings have already been described for several other species (e.g. pelargonium, apple, Pyrus) as ordinary structures in cell walls of root tissue. They have been described for varies root tissues, but never for the rhizodermis. At least, no special conditions were reported to be necessary to induce them. However, a phi layer in Ceratonia siliqua L. has been described, which was observed when plants were grown in soil but not in perlite (Praktikakis et al., 1998). In the case of Zea mays, phi thickenings were only detected in slag culture. Therefore the properties of the soil substrate were an important parameter for the presence or absence of such cell wall thickenings. The variation in the frequency of phi thickenings may be attributed to the inhomogeneity of the soil substrate. MSW slag is a heterogeneous substrate. Before use, rough particles (particle size >2 cm) were removed, but the bulk fraction still contains fragments of glass or metals and the particle size varies considerably. Thus, the bulk soil density could differ locally. Therefore, roots could be influenced only by stages in their extension. The exact reason for the presence of phi thickenings in maize grown on slag is not clear, but a relationship between the supporting role of the wall thickenings and the mechanical impedance of the soil substrate is very likely. Furthermore, the fact that the thickenings do not function as a barrier for the apoplastic movement of solutes and that they are not present around the whole root circumference suggest that they have no relevance as a barrier for solutes in the rhizodermis. This is a further argument for the mechanical supporting role, as suggested by the literature
Chemical composition of cell wall isolates
The chemical composition of hypodermal and endodermal cell walls were compared with respect to the amount of lignin, amino acids of cell wall proteins and hydrophobic compounds, because knowledge of the chemical composition of cell wall material can be usefully used to interpret the function of structural changes. Referring to the hypothesis of mechanical adaptation of roots grown in slag, the higher amount of lignin of the endodermis is a further argument. The incrustation of the cell walls with lignin is reported to provide mechanical stability for root architecture. The tight binding of lignin to the cellulose-fibrils gives high static properties to the cell walls (Richter, 1996).
Discussing the differences in lignin composition, H-enriched lignin is proposed to be stress lignin (Monties and Chalet, 1992) or lignin associated with compression wood as in gymnosperms (Campbell and Sederoff, 1996). A higher proportion of H-units produces a more condensed lignin because of more intermonomeric C–C-linkages. This functional adaptation of the hypodermis could be related to the fact that the hypodermis is the external sealing tissue of the root, which is in direct contact with the surrounding rhizosphere and its microorganisms. This fact supports the hypothesis of the contribution of the hydroxyphenyl component to the hardening of the cell walls.
Cell walls may contain both structural proteins and enzymes. The amino acid composition of these peptides can be analysed after acid hydrolysis. After the pretreatment of the cell wall material as carried out in this investigation, proteins with a structural function are assumed to remain in the cell wall because soluble or poorly bound proteins would be removed. The amino acid pattern of structural proteins varies from species to species. Monocotyledons such as maize have a threonine–hydroxyprolin-rich and a histidine–hydroxyproline-rich glycoprotein (Kieliszewski and Lamport, 1987; Kieliszewski et al., 1990). Extensin is one member of a class of hydroxyproline-rich glycoproteins (Richter, 1996). Extensin has frequently been associated with reinforcement of the cell wall network (Gladys et al., 1988). The occurrence of extensin in the sclerenchyma could be related to the mechanical function of this tissue in the plant. In addition, extensin is absent from walls of young root tissue (Gasparikova, 1992). It has been proposed that extensin contributes, with other wall components, to the tensile strength of mechanical cells.
The question arose whether or not cultivation of corn on slag, with its high content of heavy metals, causes a better exclusion of ion uptake through the apoplastic pathway by higher amounts of suberin in the hypodermis, particularly in the Casparian strips. The amount of suberin is a measure for the extent of the permeability of cell walls for water and soluble ions (Kolattukudy and Agrawal, 1974). With regard to the chromatographic results about hydrophobic compounds, it is obvious that there is no significant increase in the total amount of hypodermal suberin introduced by growing corn on slag. This indicates that there is no induction of a tighter control of apoplastic uptake by growing plants on slag. On the other hand, the higher amount of suberin in the cell wall of the hypodermis than in the cell wall of the endodermis emphasizes the role of the hypodermis as a physiological barrier for hydrophilic compounds.
Finally the results of investigations so far revealed that alterations induced by cultivation in MSW slag were of a structural nature. The roots responded to cultivation in slag with mechanical strengthening. In future, efforts will be exercised to find further physiological adaptations. Some work dealing with peroxidase activity which is involved in modifying cell wall components and detoxification of highly reactive molecules is in progress.
|
Acknowledgments |
|---|
This investigation was supported by a grant from the Graduiertenkolleg ‘Pflanze im Spannungsfeld zwischen Nährstoffangebot, Klimastreß und Schadstoffbelastung’ (B Degenhardt) and the SFB 251 (TP A2, H Gimmler). We are indebted to Lukas Schreiber for offering the opportunity for fluorescence microscopic investigations and to Jürgen Zeier for supporting gas chromatographic and mass spectrometric analysis.
|
Notes |
|---|
1 To whom correspondence should be addressed. Fax: +49 931 888 6158. E-mail:gimmler{at}botanik.uni\|[hyphen]\|wuerzburg.de
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Bennie ATP.1996. Growth and mechanical impedance. In: Waisel Y, Eshel A, Kafkafi U, eds. Plant roots, the hidden half, New York: Dekker, 453–470.
Brundrett MC, Enstone DE, Peterson CA.1988. A berberine–aniline blue fluorescent staining procedure for suberin, lignin, and callose in plant tissue. Protoplasma 146, 133–142.
Campbell MM, Sederoff RR.1996.Variation in lignin content and composition—mechanisms of control and implications for the genetic improvement of plants. Plant Physiology 110, 3 -13.[Web of Science][Medline]
Enstone DE, Peterson C.1992. The apoplastic permeability of root apices. Canadian Journal of Botany 70, 1502–1512.
Eschrich W.1995. Funktionelle Pflanzenanatomie. Berlin: Springer.
Freundl E, Steudle E, Hartung W.2000. Apoplastic transport of abscisic acid through roots of maize: effect of the exodermis. Planta 210, 221–231.
Fuchs B, Track C, Lang S, Gimmler H.1997. Salt effects of processed municipal solid waste incinerator bottom ash on vegetation and ground water. Journal of Applied Botany 71, 154–163.
Gasparikova O.1992. Root metabolism. In: Kolek J, Kozinka V, eds. Developments in plant and soil sciences, Vol. 46. Physiology of the plant root. Dordrecht: Kluwer Academic Publishers, 82–128.
Gladys I, Varner C, Varner JE.1988. Cell wall proteins. Annual Review of Plant Physiology and Plant Molecular Biology 39, 321–353.[Web of Science]
Goss MJ, Russell RS.1980. Effects of mechanical impedance on root growth in barley (Hordeum vulgare L.). Journal of Experimental Botany 31, 577–588.
Guttenberg H.1968. Der primäre Bau der Angiospermenwurzel. Encyclopedia of plant anatomy. Berlin: Gebrüder Borntraeger.
Haas DL, Carothers ZB, Robbins RR.1976. Observations on the phi thickenings and Casparian strips in pelargonium roots. American Journal of Botany 63, 863–867.
Hartung W, Zhang J, Davies WJ.1994. Does ascisic acid play a stress physiological role in maize plants growing in heavily compacted soil? Journal of Experimental Botany 45, 221–226.
Iijima M, Kono Y.1992. Development of Golgi apparatus in the root cap cells of maize, Zea mays L., as affected by compacted soil. Annals of Botany 70, 207–212.
Kolattukudy PE, Agrawal VP.1974. Structure and composition of aliphatic constituents of potato tuber skin (suberin). Lipids 9, 682–691.[Web of Science]
Kieliszewski M, Lamport DTA.1987. Purification and partial characterization of a hydroxyprolin-rich glycoprotein in a graminaceous monocot, Zea mays. Plant Physiology 85, 823–827.
Kieliszewski M, Leykam J, Lamport DTA.1990. Structure of the threonine-rich extensin from Zea mays. Plant Physiology 92, 316–326.
LAGA.1994. Technische Regeln: Anforderungen an die stoffliche Verwertung von mineralischen Reststoffen, Teil: ‘Schlacken und Aschen aus thermischen Abfallbehandlungsanlagen’ (Herausgeber Länder-Arbeitsgemeinschaft Abfall (LAGA)).
Lapierre C, Pollet B, Monties B.1991. Thioacidolysis of spruce lignin: GC–MS analysis of the main dimers recoverd after Raney nickel desulphuration. Holzforschung 45, 61–68.
Monties B, Chalet C.1992. Variability in lignification and utilization of grasses. In: Proceedings of the 14th General Meeting of the European Grassland Federation, Lahti, Finland, 111–129.
Neumann PM, Azaizeh H, Leon D.1994. Hardening of root cell walls: a growth inhibitory response to salinity stress. Plant, Cell and Environment 16, 303–309.
Peterson CA, Emanuel ME, Weerdenburg CA.1981. The permeability of phi thickenings in apple (Pyrus malus) and geranium (Pelargonium hortorum) roots to an apoplastic fluorescent dye tracer. Canadian Journal of Botany 59, 1107–1110.
Plaut Z, Newman M, Federman E, Grava A.1997. Response of root growth to a combination of three environmental factors. In: Altman A, Waisel Y, eds. Biology of root formation and development. New York: Plenum Press, 243–252.
Praktikakis E, Rhizopoulou S, Psaras GK.1998. A phi layer in roots of Ceratonia siliqua L. Botanica Acta 111, 93–98.
Reinhardt DH, Rost TL.1995. Salinity accelerates endodermal development and induces an exodermis in cotton seedling roots. Environmental and Experimental Botany 35, 563–574.
Richter G.1996. Biochemie der Pflanze. Stuttgart: Georg Thieme Verlag, 337–358.
Schreiber L, Breiner HW, Riederer M., Düggelin M, Guggenheim R. 1994. The Casparian strip of Clivia miniata Reg. roots: isolation, fine structure and chemical nature. Botanica Acta 107, 353–361.
Shannon MC, Grieve CM, Francois LE.1994. Whole plant response to salinity. In: Wilkinson RE, ed. Plant-environment interactions. New York: Dekker, 199–244.
Setia RC, Bala R.1994. Anatomical changes in root and stem of wheat (Triticum aestivum L.) in response to different heavy metals. Phytomorphology 44, 95–104.
Tessier A, Campbell PGC, Bisson M.1979. Sequential extraction procedure for the speciation of particulate trace metals. Analytical Chemistry 51, 844–851.
Tsegaye T, Mullins CE.1994. Effect of mechanical impedance an root growth and morphology of two varieties of pea (Pisum sativum L.). New Phytologist 126, 707–713.
Vepraskas MJ. 1994. Plant response mechanisms to soil compaction. In: Wilkinson RE, ed. Plant-environment interactions. New York: Dekker, 263–287.
Zeier J, Schreiber L.1997. Chemical composition of hypodermal and endodermal cell walls and xylem vessels isolated from Clivia miniata. Plant Physiology 113, 1223–1231.[Abstract]
Zeier J.1998. Pflanzliche Abschlußgewebe der Wurzel: Chemische Zusammensetzung und Feinstruktur der Endodermis in Abhängigkeit von Entwicklung und äußeren Einflüssen. PhD thesis, Universität Würzburg.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  K. Yoshimura, A. Masuda, M. Kuwano, A. Yokota, and K. Akashi Programmed Proteome Response for Drought Avoidance/Tolerance in the Root of a C3 Xerophyte (Wild Watermelon) Under Water Deficits Plant Cell Physiol., February 1, 2008; 49(2): 226 - 241. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Neuschutz, E. Stoltz, and M. Greger Root penetration of sealing layers made of fly ash and sewage sludge. J. Environ. Qual., July 1, 2006; 35(4): 1260 - 1268. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Fan, R. Linker, S. Gepstein, E. Tanimoto, R. Yamamoto, and P. M. Neumann Progressive Inhibition by Water Deficit of Cell Wall Extensibility and Growth along the Elongation Zone of Maize Roots Is Related to Increased Lignin Metabolism and Progressive Stelar Accumulation of Wall Phenolics Plant Physiology, February 1, 2006; 140(2): 603 - 612. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
X. Wu, J. Lin, Q. Lin, J. Wang, and L. Schreiber Casparian Strips in Needles are More Solute Permeable than Endodermal Transport Barriers in Roots of Pinus bungeana Plant Cell Physiol., November 1, 2005; 46(11): 1799 - 1808. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. Hose, D.T. Clarkson, E. Steudle, L. Schreiber, and W. Hartung The exodermis: a variable apoplastic barrier J. Exp. Bot., December 1, 2001; 52(365): 2245 - 2264. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||