Journal of Experimental Botany, Vol. 54, No. 381, pp. 335-344,
January 2, 2003
© 2003 Oxford University Press
Xyloglucan endotransglucosylase action is high in the root elongation zone and in the trichoblasts of all vascular plants from Selaginella to Zea mays
Received 9 April 2002; Accepted 26 August 2002
1 Laboratory of Plant Physiology and Morphology, Department of Biology, University of Antwerp (UIA), Universiteitsplein 1, B-2610 Wilrijk, Belgium
2 Edinburgh Cell Wall Group, Institute of Cell and Molecular Biology, The University of Edinburgh, Daniel Rutherford Building, The King’s Buildings, Edinburgh EH9 3JH, UK
3 To whom correspondence should be addressed. Fax: +32 3 820 2271. E-mail: Jean-pierre.verbelen{at}ua.ac.be
Abbreviations: GAX, glucuronoarabinoxylan; XET, xyloglucan endotransglucosylase (=name of enzyme activity or action); XGO-SR, sulphorhodamine-labelled xyloglucan oligosaccharide; XTH, xyloglucan endotransglucosylase/hydrolase (=name of protein); XyG, xyloglucan.
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Abstract |
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The endotransglucosylase action of the enzyme xyloglucan endotransglucosylase/hydrolase (XTH) was localized in the roots of diverse vascular plants: club-mosses (lycopodiophytes), ferns, gymnosperms, monocots, and dicots. High action was always found in the epidermis cell wall of the elongation zone and in trichoblasts in the differentiation zone. Clearly XTH and its action in root development evolved before the evolutionary divergence of ferns and seed plants and also of the lycopodiophytes and euphyllophytes.
Key words: Club-mosses, ferns, roots, seed plants, xyloglucan endotransglucosylase/hydrolase (XTH).
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Introduction |
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In higher plants, cells are surrounded by a wall, which defines the cell’s shape and thereby contributes to the structural integrity and morphology of the entire plant. The growing cell wall of flowering plants consists of cellulose microfibrils embedded in a matrix of hemicelluloses, pectins and glycoproteins (Fry, 1986; Carpita and Gibeaut, 1993; Darvill et al., 1980; McNeil et al., 1984; McCann and Roberts, 1991; Pauly et al., 1999).
Depending on their polysaccharide composition, walls are divided into two types. Dicotyledons have a ‘type I’ primary cell wall. Typically, xyloglucans (XyG) are the major hemicellulose. They coat and probably tether adjacent cellulose microfibrils, thereby forming the load-bearing cellulose/XyG network (Fry, 1989; Carpita and Gibeaut, 1993; Pauly et al., 1999). Xyloglucans also form covalent linkages to rhamnogalacturonans (Thompson and Fry, 2000), so that part of the cellulose/xyloglucan network is bonded to, and not independent of, the pectic network. Monocotyledons can be divided in two groups depending on the presence or absence of ester-linked ferulic acid in their primary cell walls. The group containing ferulic acid is identical to the commelinoid group of monocotyledons identified in cladograms using the rbcL gene (Chase et al., 1993; Duvall et al., 1993). The composition of a non-commelinoid cell wall is similar to that of the ‘type I’ cell wall found in dicotyledons. In the commelinoid group the cell walls of Poales families contain XyG and pectins in relatively low amounts, glucuronoarabinoxylans (GAXs) in higher amounts and mixed-linkage ß-D-glucans [(1
3,14)-ß-glucans] in variable amounts (Carpita, 1996). These walls are called ‘type II’ walls. The cell walls of other commelinoids lack the (13,14)-ß-glucans and have polysaccharide compositions intermediate between Poales and non-commelinoids (Carpita and Gibeaut, 1993; Smith and Harris, 1999; Harris, 2000). Knowledge on the architecture and composition of the primary cell wall in pteridophytes is fragmentary (Popper et al., 2001), probably because they are not commercially interesting world crops.
Plant cell expansion needs the movement or slippage of cellulose microfibrils in response to turgor-driven mechanical forces (Cosgrove, 1997a). Enzymatic modification of the tethering XyG, resulting in cell wall loosening, is considered a key process necessary for cell expansion (Fry, 1989, 1995). Two families of proteins, expansins and xyloglucan endotransglucosylase/hydrolases (XTHs), are considered to play an important role in this process. Expansins are presumed to loosen in a non-hydrolytic way the cellulose–XyG bonds. The primary enzyme activity of XTH proteins is xyloglucan endotransglucosylase (XET), the cutting and rejoining of XyG chains (Fry et al., 1992; Nishitani and Tominaga, 1992; Rose et al., 2002), which may cause wall loosening both by enabling the integration of newly secreted xyloglucans into the wall and by restructuring existing wall-bound xyloglucans (Thompson and Fry, 2001). Depending on the substrate conditions, some XETs may also cause hydrolysis of XyG (Fanutti et al., 1993). In Arabidopsis the XTH gene family contains 33 genes with different expression patterns (Yokoyama and Nishitani, 2001). A fluorescent technique was recently developed that enables specific visualization of transglucosylation (XET action) mediated by XTH, not of the enzyme’s hydrolytic action. An exogenous fluorescently labelled xyloglucan oligosaccharide (XGO-SR) becomes incorporated into the cell wall at sites where XTH acts on endogenous XyG. In Arabidopsis high XET action is confined to the elongation zone of the root (Vissenberg et al., 2000), to expanding cells in other organs (Verbelen et al., 2001) and to the site of future root hair initiation (Vissenberg et al., 2001). High XET action was also detected in expanding cells of other dicotyledonous plants (Verbelen et al., 2001).
The expansin multigene family was formed before the evolutionary divergence of ferns, monocotyledons and dicotyledons (Shcherban et al., 1995; Kim et al., 2000). The presence of XET action in selected species of all classes of vascular plants, including pteridophytes was investigated. This study reports on the general occurrence of XET action in roots of pteridophytes and seed plants, and maps the sites with high XET action relative to the elongation zone.
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Materials and methods |
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Plant cultures
Representatives of different vascular plant families (Table 1) were grown in soil or in vermiculite and kept in a culture room at 22 °C in a 16 h photoperiod (light intensity 24 µmol m–2 s–1; Philips tlm 65W/33). The plants in Table 1 marked with an asterisk were a gift from the National Botanical Garden of Belgium; the others were collected in the campus environment or bought in local shops. The classification used in Table 1 is according to the angiosperm phylogeny group with recent minor corrections for some families of the monocotyledons (APG, 1998; Chase et al., 2000. See also http://www.biologie.uni-hamburg.de/ b_online/apg/APG.html).
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Cytochemical assay
The XET action of XTH was demonstrated as described by Vissenberg et al. (2000). In brief, healthy roots were incubated in a 6.5 µM XGO–SR mixture (XLLG–SR > XXLG–SR > XXXG–SR; see Fry et al. (1993) for nomenclature and Fry (1997) for the synthesis) dissolved in MS culture medium at pH 5.5 for 1 h. The assay was followed by a 10 min wash in ethanol/formic acid/water (15:1:4, by vol.) and an incubation overnight in 5% (w/v) formic acid. A solution of cellobiose–SR (= non-XTH substrate) was used also at a concentration of 6.5 µM as a control for assays of XET action.
Fluorescence analysis
Fluorescence pictures of small roots were made using the 514 nm laser line of a Bio-Rad MRC 600 confocal laser scanning microscope mounted on a Zeiss Axioskop and equipped with a 40x water immersion objective (NA 0.9) and a 10x objective (NA 0.3). Fluorescence pictures of large roots were made using a Nikon DXM1200 digital camera mounted on a Leitz Orthoplan (Wetzlar, Germany) fluorescence microscope using green (540 nm) excitation light and a 4x objective (NA 0.14).
Roots assayed with XGO-SR or cellobiose-SR (=control assay) were visualized using identical settings of the confocal microscope (laser intensity, pinhole, gain, and black level) or the digital camera (exposure time) to enable comparison of the fluorescence.
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Results |
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For convenience, the root tip always points to the bottom in all figures, except in Fig. 1 and in Fig. 5 where the root tip is situated at the right side of the figures. The XET action of XTH was assayed in roots of 61 different species belonging to 33 different families of the plant kingdom (Table 1). In all species tested high XET action was involved in root hair development. In all species but one (family Arecaceae) the root elongation zone exhibited a higher XET action than the non-elongating zone. Not all data can be displayed in this paper. Only a selection of representative species is shown. The other pictures can be found on the following web-site: http://www.uia.ac.be/bio/fymo/JExpBot2002.html.
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XTH action is present in roots of the most primitive vascular plants
Figure 1A shows a dichotomously branching root of Selaginella, a club-moss. The fluorescence is caused by the incorporation of fluorescently labelled XyG-oligosaccharides into the cell wall by the XET action of XTH. The roots of this primitive vascular plant exhibit clear XET action in the zone of fast cell elongation. In control roots, where a fluorescent non-XTH substrate (cellobiose-SR) was used (Fig. 1B), the elongation zone exhibits no increased fluorescence at all. The fluorescence in Fig. 1A is therefore indicative of the XET action of XTH.
In all true ferns (Polypodiopsida) assayed, the control experiments yielded substantial autofluorescence. Particularly when roots were studied at low magnification, the XET-related fluorescence was difficult to visualize against this background. Fig. 1C and D show the XET assay and the control in the aquatic fern Microsorum pteropus. There is a substantial difference due to XET-caused fluorescence especially in the zone of rapid elongation. At higher magnification it is clear that cell walls are much more fluorescent in the XET-assayed roots (Fig. 1E, G) than in the control roots (Fig. 1F, H). XET-action is thus clearly present in the fast elongation zone of fern roots.
XET action in roots of gymnosperms
Although detection of XET action in pteridophytes and angiosperms encountered no major problems, the majority of gymnosperm roots were problematic in this respect. The roots appeared to be encapsulated in a very long and thick root cap, which prevented the epidermal cells from being assayed with the XGO–SRs. Figure 2A is a representative example showing the root of Picea abies after the XET assay. Even with the confocal microscope, no clearly delineated epidermal cells could be detected. The only species that had a short root cap was Taxus baccata. In this species too XET action was clearly present in the elongation zone (Fig. 2B) when compared to the control (Fig. 2C).
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XET action is present in roots of all angiosperms
Figure 2D and E represent the XET action of XTH in roots of a species of the Piperales, a group of plants of the angiosperms that is not finally assigned to the monocotyledons nor to the dicotyledons. The epidermal cell walls of the Pothomorphe petalta root clearly contain XTH enzymes that act on endogenous donor substrate (Fig. 2D) whereas the control root, with cellobiose-SR, displays no appreciable fluorescence (Fig. 2E).
In all roots of mono- and dicotyledons high XET action was especially confined to the rapidly elongating region of the root. However, the length of the zone with high XTH action differed among the different species assayed. The control assays gave no appreciable background fluorescence and are shown for Iris (Fig. 3B), Vulpia (Fig. 3F) and Lactuca (Fig. 3K). Figure 3A, C and D represent XET action in non-commelinoid monocotyledons (A, C and D are Iris pseudacorus, Lemna minor and Aloe sp., respectively), Fig. 3E, G, H, and I in commelinoid monocotyledons (Vulpia myuros, Triticum dicoccum, Beckmannia syzigachne and Commelina nilagirica, respectively) and Fig. 3J, L, M and N represent Lactuca perennis, Cochlearia officinalis, Blumenbachia hieronymi, and Nicotiana tabacum, respectively, a selection of dicotyledons. Generally the intensity of XET action in the elongation zone decreased slowly in cells further away from the tip. However, in some commelinoid monocotyledons (Pitcairnia, Cenchrus, Vulpia (Fig. 3E), Luzula, and Carex), the enzyme’s action dropped drastically at the end of the elongation zone. In these roots the zone with very high XET action was rather short; the roots were smaller and exhibited lower growth rates when compared to other roots with a larger ‘high XET action’ zone (results not shown). This abrupt drop in XET action was never observed in roots of dicotyledons or non-commelinoid monocotyledons.
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Within the monocots, the roots of Chamadorea elegans, a palm, were peculiar. Figure 4A and B exhibit no significant difference in fluorescence intensity between XET assayed roots (A) and controls (B). In these roots there is no real elongation zone. Epidermis cells only elongate until their outer surface becomes approximately square, their length being equal to their width. However, a limited XET action was found in root hair cell walls.
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High XET action in trichoblasts
In a previous paper (Vissenberg et al., 2001) another site of high XET action in Arabidopsis roots was reported: in trichoblasts the enzyme’s action denoted the sites of future root hair emergence and was present in the growing root hair cell wall. The remainder of the trichoblast cell wall did not exhibit high XET action. This type of localized XET action was also found in the majority of the roots studied here (Fig. 5A). In some species, however, high action occurs in the whole trichoblast cell wall whereas atrichoblasts lack this enzymatic action (Fig. 5B). Cochlearia, a member of the Brassicaceae, exhibits this second type of XET action in trichoblasts. In the Brassicaceae, the trichoblast cell files are clearly separated by non-fluorescent atrichoblast cell files as each cell file consists of only one type of cell, either all bearing or all not bearing root hairs (Dolan, 1996). A comparable situation is found in some commelinoid monocotyledon species like Briza, Beckmannia, Canna, and Commelina. Again the trichoblasts exhibit high XET action in the complete cell wall, but trichoblasts and atrichoblasts are not found in clearly separated cell files. In these species any cell seems capable of acquiring the trichoblast identity (Fig. 5C). Also in Selaginella high XET action was found in the cell walls of trichoblasts (Fig. 5D).
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Discussion |
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In Arabidopsis high XET action delineates the elongation zone of the root and also marks the onset of trichoblast differentiation (Vissenberg et al., 2000, 2001), suggesting a role in cell elongation. In maize roots, the peak of extractable XTH (assayed in vitro as XET activity, as distinct from XET action) was 3 mm from the root tip, slightly distal to the peak of local elemental relative elongation rate (5 mm from the tip; Pritchard et al., 1993), suggesting that XET plays a role in wall assembly as well as loosening, and/or that XTHs are present in the tissue before they begin to act. To explore the evolutionary history of XTH, the enzyme’s action was assayed in roots of many different species including club-mosses, ferns, gymnosperms, monocotyledons, and dicotyledons.
The XET action of XTHs was detectable in all classes of pteridophytes and spermatophytes. This is an indication that the development and expression of XTH genes preceded the evolutionary divergence of ferns and seed plants. In this respect, XTH genes mirror the occurrence of the expansin multigene family in the plant kingdom (Kim et al., 2000; Shcherban et al., 1995). XET action was even detected in Selaginella, a club-moss. Club-mosses diverged early from the ancestors of the euphyllophytes (= plants with ‘true’ leaves, being all seed plants as well as non-club-moss pteridophytes) (Chaw et al., 1997; Duff and Nickrent, 1999; Qiu and Palmer, 1999; Vangerow et al., 1999; Wolf, 1997). A further proof of the isolated evolutionary position of the club-mosses is an unusual sugar residue, 3-O-methyl-D-galactose, found only in the club-moss cell wall (Popper et al., 2001). Extractable XET activity has also been detected in bryophytes such as the liverwort Marchantia (both sporophyte and gametophyte) and the moss Mnium (Fry et al., 1992). However, in these non-vascular land plants, which lack roots, the histological distribution of XET action has not been studied. Furthermore, although acid growth has been observed even in some green algae (Cosgrove, 1997b), suggesting a mechanism of cell expansion shared with angiosperms, recent studies have shown that the charophytes Chara, Klebsormidium and Coleochaete (probably among the closest living algal relatives of the land plants) do not possess xyloglucan (ZA Popper, SC Fry, unpublished results); XTH would therefore seem unlikely to occur in plants lower than bryophytes. In this report, the study was limited to the detection of XET action of XTHs in roots. It can, therefore, be stated that whenever roots are growing in the plant kingdom, even in the most primitive vascular land plants, XET action is present. This wall expansion mechanism may be deeply embedded in the evolution of land plants.
In dicotyledons, where XyG is the major tethering hemicellulose in the cell wall, the action of XET during cell elongation can be imagined. For microfibrils to move apart or past one another, the tethering XyG needs to be modified, probably by the concerted action of expansins (Cosgrove, 2000), XTHs (Fry et al., 1992; Vissenberg et al., 2000) and endo-glucanases (Nicol et al., 1998), and possibly hydroxyl radicals (Fry, 1998; Schopfer, 2001). XTHs alone (unlike expansins alone) were not able to promote creep in heat-killed, stretched, cucumber hypocotyls (McQueen-Mason et al., 1993); however, negative evidence in an assay optimized for expansin action does not disprove the ability of XTHs to promote wall loosening. For example, it remains to be shown whether exogenous XTHs can adequately permeate the wall matrix. In monocotyledonous species with very low XyG content and GAXs and (13,14)-ß-glucans as major tethering polysaccharides (Carpita and Gibeaut, 1993), high XET action is more surprising. As extraction of XyG with mild alkali is greatly improved by conditions where etherified and esterified phenolics are cleft (Carpita, 1986), it is very well possible that XyG is cross-linked to other wall polysaccharides and that XTH plays a role in the restructuring of the XyG in this polysaccharide network (Thompson and Fry, 2000, 2001). A related explanation, suggested by Yuan et al. (2001), could be that two polysaccharide networks might coexist and that they tether microfibrils in parallel. Therefore, both networks need to be loosened to result in significant wall expansion. Using this technique, it is not possible to distinguish between endotransglycosylase action on XyG or on the GAXs and the (13,14)-ß-glucans. As no polysaccharide other than XyG has been shown to be substrate for XTH (Fry et al., 1992; Wu et al., 1994) it can only be assumed that only the XET action of XTH on the XyG/cellulose network has been shown.
All ferns and lycopodiophytes tested have been found to possess xyloglucan (ZA Popper, SC Fry, unpublished results). As XET was found to act in the roots of all pteridophytes tested (present paper), and as expansin genes (Shcherban et al., 1995) and probably expansin proteins (Kim et al., 2000) are present in ferns, and as the mRNA for an extensin that exhibits great structural similarities to dicot and monocot extensins is synthesized in spores of the fern Adiantum (Uchida et al., 1998), it seems likely that pteridophyte cell walls function in ways quite similar to those of angiosperms.
High XET action was also typical of differentiating trichoblasts in all plants studied. In the majority of the species, high XET action was localized specifically to the site of root hair initiation whereas the rest of the cell wall was devoid of this action, as was reported for Arabidopsis (Vissenberg et al., 2001). In some commelinoid monocotyledon species XET action was high throughout the entire trichoblast cell wall. Nevertheless, root hairs in these plants were formed at the correct sites. This can be explained by the fact that root hair initiation and emergence are multifactorial processes. While in the cytoplasm Rop GTPase proteins (Molendijk et al., 2001), profilin and F-actin (Braun et al., 1999) are important during root hair growth, different cell wall loosening factors such as XTH (Vissenberg et al., 2001) and expansin (Balu
ka et al., 2000) might be involved in defining the growth of certain wall domains in the trichoblast and later in the root hair. The correct site of root hair emergence could then be defined by the action of expansin itself being activated by a local acidification of the wall (Bibikova et al., 1998). Clearly XET action of XTHs is a faithful marker for trichoblast differentiation, and may be necessary for root hair growth, but is not sufficient to initiate root hair growth.
To conclude, it can be stated that the emergence of XET action of XTHs preceded the evolutionary divergence of lycopodiophytes, ferns and seed plants. These results provide strong evidence for a general association of XET action with cell elongation and with trichoblast differentiation in roots.
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Acknowledgements |
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Kris Vissenberg is Postdoctoral Fellow of the Fund for Scientific Research (FWO), Flanders (Belgium) and Vicky Van Sandt is an undergraduate student. The confocal laser scanning microscope was supported by the Fund for Scientific Research, Flanders (grants nos 3.0028.90, 2.0049.93, and G.0034.97). This work was supported by the Biotechnology and Biological Sciences Research Council, UK (research grant to Stephen C Fry). The authors thank the National Botanical Garden of Belgium for the generous gift of seeds.
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