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(American Journal of Botany. 2008;95:655-663.) doi: 10.3732/ajb.2007368 © 2008 Botanical Society of America, Inc. |
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Cell Biology |
Southern Weed Science Research Unit, Agricultural Research Service, P.O. Box 350, U.S. Department of Agriculture, Stoneville, Mississippi 38776 USA
Received for publication 16 November 2007. Accepted for publication 13 March 2008.
ABSTRACT
Gelatinous fibers (G-fibers) are the active component of tension wood. G-fibers are unlike traditional fiber cells in that they possess a thick, nonlignified gelatinous layer (G-layer) internal to the normal secondary cell wall layers. For the past several decades, the G-layer has generally been presumed to be composed nearly entirely of crystalline cellulose, although several reports have appeared that disagreed with this hypothesis. In this report, immunocytochemical techniques were used to investigate the polysaccharide composition of G-fibers in sweetgum (Liquidambar styraciflua; Hamamelidaceae) and hackberry (Celtis occidentalis; Ulmaceae) tension wood. Surprisingly, a number of antibodies that recognize arabinogalactan proteins and RG I-type pectin molecules bound to the G-layer. Because AGPs and pectic mucilages are found in other plant tissues where swelling reactions occur, we propose that these polymers may be the source of the contractile forces that act on the cellulose microfibrils to provide the tension force necessary to bend the tree trunk.
Key Words: arabinogalactan proteins • cell walls • Celtis occidentalis • gelatinous fibers • immunocytochemistry • Liquidambar styraciflua • rhamnogalacturonan I • tension wood
Trees use gravitropic and phototropic responses to orient their trunks and branches so that their leaves can gather sunlight. To achieve and maintain these orientations, angiosperms have evolved specialized wood tissue that forms on the upper surface of branches and leaning trunks that has the ability to exert a contractile force (Scurfield, 1973
). This wood is called tension wood because it is normally under tension as gravity pulls on the leaning trunk or branch and because it exerts a tensile force that can pull a tree trunk vertical or hold a large branch horizontal. Tension wood is of special interest to humans because its presence in lumber causes the wood to warp as it dries, reducing its usefulness and therefore its value.
Tension wood cells are characterized by the presence of a gelatinous layer (G-layer) and are therefore referred to as gelatinous fibers (G-fibers). It is generally believed that the G-layer is composed of (nearly) pure cellulose (Norberg and Meier, 1966). However, this layer may contain polysaccharides including pectin and hemicellulose in addition to cellulose (Scurfield, 1972; Furuya et al., 1970). Evidence of xyloglucan and xyloglucan-synthesizing proteins in the G-layer has also been reported (Nishikubo et al., 2007). Also, two groups, using entirely different techniques, have reported that arabinogalactan proteins (AGP) are likely to be present in the G-layer (Lafarguette et al., 2004; Andersson-Gunnerås et al., 2006).
Animals exert forces on their skeletons with muscles. The muscle cells use energy to contract. Unlike the muscle cells of animals, however, the wood cells of trees are dead at maturity and thus are not able to use energy to generate movement. Tension wood is well known to shrink upon drying (e.g., Norberg and Meier, 1966). By including polysaccharides that change size with changing moisture content in the walls of tension wood, trees are able to exert force with (essentially) dead tissue.
Recently, tendrils of the weed vine Brunnichia ovata (redvine) were shown to contain G-fiber-like cells, which are thought to play a role in maintaining the coiled position of tendrils by utilizing a tension-generating mechanism analogous to that used by tension wood in angiospermous trees (Meloche et al., 2007). Using immunocytochemical methods, Meloche et al. discovered that the G-layers of these cells contained arabinan and galactan, which frequently occur as side chains of rhamnogalacturonan I (RG I). Here, a similar immunolabeling approach was used to determine the polysaccharide composition of the cell walls of both normal wood and tension wood of sweetgum (Liquidambar styraciflua L.; Hamemm) and hackberry (Celtis occidentalis L.). Our data indicated that G-fibers contain significant quantities of RG I, arabinogalactan (AG), and AGP. We suggest that these noncellulosic polysaccharides in the G-layer may be the source of the force generated by tension wood.
MATERIALS AND METHODS
Plant material and specimen preparation
Tension wood was collected from the upper surface of conspicuous bends in the trunk of two different sweetgum (Liquidambar styraciflua; Hamamelidaceae) trees and a hackberry (Celtis occidentalis; Ulmaceae) tree growing in a bottomland forest maintained by Mississippi State University, Stoneville, Mississippi, USA. The bark was removed from a square region above the bend, then a square of wood 
1 x1 cm was removed with a sharp chisel. The wafer of wood was immediately immersed in water at the site and transported to the laboratory. Wood was prepared in a manner similar to that described by Clair et al. (2005). Using fine forceps and a razor blade, the wafer was split along the grain into splinters c. 1 mm per side and 1 cm long. These splinters were then cut with a new razor blade, in 3% glutaraldehyde in 50 mM 1,4 piperazine-bis-(ethanesulfonic acid) (PIPES), pH 7.2, into 1 x 1 x 0.5 mm slices. Wood samples were fixed for 2 h at room temperature and then washed several times with 50 mM PIPES. Samples were dehydrated at room temperature in 25, 50, and 75% (2 h each) ethanol and absolute ethanol overnight, then infiltrated with increasing concentrations of LR white resin (Polysciences,Warrington, Pennsylvania, USA) in ethanol (25, 50, 75, 100%, 24 h each), also at room temperature. Specimens in 100% resin were placed onto a shaking platform for 48 h. Slices were placed into cylindrical polyethylene capsules (Ted Pella, Redding, California, USA) and polymerized at 55°C for 2 h. Sections (0.55 µm) were cut on a Reichert (Vienna, Austria) UltraCut E microtome and stained with 1% toluidine blue (in 1% sodium borate) and imaged on a Zeiss (Jena, Germany) Axioskop with an Olympus (Tokyo, Japan) Q-color 3 digital camera. Images were contrast-enhanced with the program ImageJ (National Institutes of Health, Bethesda, Maryland, USA) and made into plates using the program GIMP (version 2.2; http://www.gimp.org/).
Immunogold-silver staining for light microscopy
Semithin sections (550 nm) were blocked with 1% (w/v) BSA in phosphate-buffered saline (PBS) for 30 min at room temperature. Primary antibody was applied to sections (at various dilutions in PBS-BSA) and incubated in a moist chamber for 3 h. Each antibody application was repeated at least once, on two different days. CCRC-series antibodies were purchased from Carbosource, Complex Carbohydrate Research Center, University of Georgia, Athens, Georgia, USA. The JIM-series and the LM-series antibodies were purchased from Plant Probes (Leeds, UK). Sections were rinsed and incubated with secondary antibody (15 nm gold, E-Y Laboratories, San Mateo, California, USA) diluted 1:20 in PBS-BSA for 1 h at room temperature. Sections were silver-enhanced (Amersham IntenSE, GE Healthcare, Buckinghamshire, UK) for 20–30 min at room temperature. Images were collected as for light microscopic sections.
RESULTS
Structure of sweetgum tension wood–normal wood interface
Thin sections of tension wood from sweetgum embedded in LR white were stained with toluidine blue (Fig. 1). Three different types of cells can be discerned (Fig. 1C): normal wood cells to the left, "transition zone" cells in the middle, and tension wood cells to the right. Tension wood cells can be easily identified by the presence of a conspicuous pink-red layer internal to the much thinner light purple-blue secondary wall (Fig. 1C and D). The normal wood cells have thick, dark-purple middle lamellae and light-purple-blue secondary walls. The cells of the transition zone between normal and tension wood have much thinner middle lamellae and much thicker purple-blue secondary walls.
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, and references therein; Hsu et al, 2005).
Immunocytochemical investigation of G-fibers of sweetgum
Sections containing G-fibers were probed with 27 different antibodies raised to various plant cell wall polysaccharides. The levels of reaction of the various antipolysaccharide antibodies to different cell types and subwall regions of tension wood have been scored (Table 1).
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Xylans were found to be present primarily in the secondary cell walls (S1 and S2 layers) of G-fiber cells. Xylans were localized with LM10 (de-arabinosylated xylan; Fig. 2K) and LM11 (xylan/arabinosylated xylan; not shown). A clear zone, corresponding to the location of the G-layer, can be seen between the LM10 labeling and the sporadic/punctate labeling found in the cell lumen. Also, a much thinner clear zone can be seen in the area of the middle lamella/primary wall. Thus, xylans appear to be present in only the S1 and S2 layers, but not the G-layer or primary wall. JIM13 (AG/AGP/RG I; Fig. 2E) and JIM15 (AG/AGP; Fig. 2F) were also found to bind to the S1 and/or S2 layers of G-fibers, although these antibodies did not label these cells as strongly as the antixylan antibodies LM10 and LM11. The AG/AGP epitope recognized by JIM15, in particular, was present in very limited quantities in the S1 layer. None of the antibodies used in this study labeled both the S1/S2 layers and the G-layer; the polysaccharide components of these layers appeared to be mutually exclusive, at least with the antibodies used in this study.
Fucosylated xyloglucan (CCRC-M1; Fig. 2A) was present in the middle lamella and (perhaps) the primary cell wall, but not in cell corners. It should be noted that the epitope recognized by CCRC-M1 may also be present, albeit to a lesser extent, on some types of RG I molecules (Complex Carbohydrate Research Center, 2007). This epitope was present in the terminal lamella (Fig. 2A, arrowheads), although it is unclear whether it is part of an RG I or a xyloglucan.
Highly de-esterified homogalacturonan (JIM5; Fig. 2B) and pectic mucilage (CCRC-M38; Fig. 2C) appeared to be present only in the middle lamella/primary wall of both G-fiber cells and normal wood cells. It seems likely that JIM5-reactive homogalacturonans are present only in the middle lamella region and not in the walls, per se, just as they are in other systems.
CCRC-M38-reactive mucilage and CCRC-M1-reactive fucosylated xyloglucan were found on the luminal edge of the G-layer (Fig. 2C, arrowhead), but not in the G-layer itself. This layer appears to correspond to the so-called "terminal lamella" reported by Cote et al. (1969) and Scurfield (1972). As mentioned, RG I epitopes (recognized by CCRC-M7, Fig. 2G; CCRC-M10, Fig. 2H; and CCRC-M22, Fig. 2I) were found in large amounts in the G-layer, and this RG I-containing zone may include the terminal lamella. However, because the terminal lamella is directly adjacent to the G-layer, this determination is very difficult to make.
Nonfucosylated xyloglucan appeared primarily in the walls of vessels, tyloses, rays, and normal wood cells, and was largely absent from the walls of G-fibers, with the exception of some very weak primary wall labeling (LM15; Fig. 2L). This localization is in marked contrast to fucosylated xyloglucan, which, as mentioned, was also present in the early walls of G-fibers (CCRC-M1; Fig. 2A).
Immunocytochemistry of G-fibers of hackberry
Because our observations of G-fibers in sweetgum seemed to be in such stark contrast to previously published studies, tension wood from a nonrelated tree, hackberry, was also probed with a battery of antipolysaccharide antibodies (Fig. 3). The patterns of localization in the two species for all the antibodies tested were nearly identical. As in sweetgum, antibodies to RG I (CCRC-M10 and CCRC-M22) were found to bind the most exclusively to the G-layer (Fig. 3A–C). Also, the anti-AGP antibody, JIM13, and the antixylan antibody, LM10, bound primarily to the S1/S2 layers (Fig. 3D and 3F), and the antifucosylated xyloglucan antibody, CCRC-M1, labeled the ML/primary wall (Fig. 3E).
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DISCUSSION
Arabinogalactans and arabinogalactan proteins in the gelatinous layer
Of the five antibodies that labeled the G-layer, three (JIM14, CCRC-M7, and CCRC-M34) are known to recognize AG/AGP (Complex Carbohydrate Research Center, 2007). These findings agree with recent reports indicating that AGPs are present in the G-layer of Populus spp. (Lafarguette et al., 2004; Andersson-Gunnerås et al., 2006). In one study, JIM14 was found to bind to an inner layer of developing (2-mo-old) G-fibers (Lafarguette et al., 2004). In the present study, tension wood from a layer 1–3 yr old was analyzed, and JIM14 extensively labeled the entire G-layer (Fig. 2D). It is possible that, as the G-layer matures, AGPs are continuously being released from the surface of the plasma membrane and thus build up in the G-layer.
In addition to their normal role as anti-AGP reagents, both JIM14 and CCRC-M7 have also been found to bind to RG I isolated from sycamore maple (Acer pseudoplatanus) (Complex Carbohydrate Research Center, 2007). Furthermore, CCRC-M34 was raised to Arabidopsis seed coat mucilage (largely composed of RG I). Therefore, it is unclear whether the epitopes recognized by these antibodies are present as side-chains of RG I or as free AGP.
Immunocytochemical evidence for rhamnogalacturonan I in the gelatinous layer
Four of the five antibodies that bind the G-layer (CCRC-M7, CCRC-M10, CCRC-M22, and JIM14) recognize epitopes on RG I molecules (Complex Carbohydrate Research Center, 2007). CCRC-M7 recognizes RG I as well as both soluble and membrane-bound AGPs. CCRC-M22 and CCRC-M10 recognize epitopes on RG I. JIM14 was raised to AGP2, but binds to RG I from sycamore maple as well. Only CCRC-M34 is not explicitly described as binding to RG I, but, as mentioned, this antibody was actually raised to seed coat mucilage.
RG I is composed of a repeating rhamnose (Rha), galacturonic acid (GalA) disaccharide backbone. The Rha residues of RG I may have three different types of side chains attached to them: arabinan, galactan, and type I arabinogalactan (Carpita and McCann, 2000). Type I arabinogalactan is a backbone of galactan with arabinan side chains. In sweetgum, neither LM5 (anti-1,4 galactan side chain) nor LM6 (anti-1,5 arabinan side chain) antibodies labeled the tension wood in any appreciable amount (Table 1). This means that if RG I molecules are present, they do not have arabinan or galactan side chains. A similar RG I backbone without arabinan or galactan side chains was observed in the adhesive of the Virginia creeper tendril (Bowling and Vaughn, in press).
Because CCRC-M22 was raised to de-arabinosylated (but not de-galactanated) RG I and type I AGs have a galactan backbone, the binding of CCRC-M22 to RG I, which bears type I arabinogalactan side chains, seems plausible. However, as demonstrated here, LM5 does not recognize the 1,4 galactan backbone of these type I AG side chains. Thus, CCRC-M22 may actually bind to the RG I backbone. That CCRC-M10, which is also described as binding to RG I, recognizes the G-layer in a pattern almost identical to CCRC-M22, strongly indicates the presence of RG I.
Although CCRC-M22 and CCRC-M10 probably both recognize RG I backbone epitopes, the results of this and a previous study indicate that these antibodies recognize related, but different types of RG I molecules. In Virginia creeper (Parthenocissus quinquefolia), CCRC-M22 and CCRC-M10 recognized similar but distinctly different regions in the adhesive tendril pad (Bowling and Vaughn, in press). Similarly, in the current study, CCRC-M22 appeared to recognize a minor component of the compound primary wall/middle lamella, while CCRC-M10 had no reactivity to it (e.g., Figs. 2G, H).
In summary, five different antibodies recognized the G-layer. Four of these antibodies are known to recognize RG I, and the fifth, although not described as binding RG I, was originally raised to seed coat mucilage. Two of these antibodies are thought to recognize the backbone of RG I, but not to recognize AGP. However, three of these five antibodies are also described by their supplier as binding to AGP, which corresponds with other recent studies indicating the presence of AGPs in G-fibers (Lafarguette et al., 2004) and tension wood (Andersson-Gunnerås et al., 2006). For these reasons, both RG I and AGP are likely to be in the G-layer.
Further evidence for RG I in the G-layer
Toluidine blue O is well known to stain acidic polysaccharides pink-red (O’Brien et al., 1964; Gahan, 1984). As shown in Fig. 1, the G-layer of sweetgum tension wood stains a pink-red color with toluidine blue O, thus indicating the presence of acidic polysaccharides in this layer. This pink-red color is a characteristic of G-layers (Krishnamurthy, 1999) and has been seen in other species (e.g., Hsu et al., 2005). HG and RG I are the predominant acidic pectins in plant cell walls (Carpita and McCann, 2000). However, because we see no binding of the G-layer by either de-esterified HG antibodies (JIM5) or partially de-esterified antibodies (JIM7), the presence of significant amounts HG in the G-layer seems unlikely. Thus, the most logical conclusion is that RG I is the component of the G-layer reacting with toluidine blue, although the presence of an (as yet uncharacterized) acidic AG/AGP cannot be completely ruled out.
Ruthenium red is another known reagent for staining pectins (Gahan, 1984; Sterling, 1970;Krishnamurthy, 1999). The G-layer of Eucalyptus stains very strongly with ruthenium red, thus indicating the presence of acidic pectins in this layer (Scurfield, 1972). However, the author was unwilling to say definitively that acidic pectins were present because only cellulose was present according to other studies at the time (Norberg and Meier, 1966). As another, more indirect indication that the G-layer may contain pectins similar to those found around seeds is the observation that tension wood embedded in methacrylate can swell to a large degree when placed into water (Cote et al., 1969). Others have described the G-layer as highly hygroscopic and that it swells in water to fill the lumen of the G-fiber (Evert, 2006). This swelling in water is a known property of seed coat mucilage, but not of pure cellulose, and de-branched RG I is the major component of the seed coat mucilage of Arabidopsis (Macquet et al., 2007).
Furuya et al. (1970) also reported the presence of pectins in the G-layer. This group isolated G-layers by the same sonication technique that was used by Norberg and Meier (1966). After complete hydrolysis of the isolated G-layers in sulfuric acid, they found xylose, mannose, galactose, arabinose, and galacturonic acid residues in addition to glucose. As mentioned, antibodies to HG (JIM5 and JIM7) did not react with the G-layer. However, the backbone of RG I also contains galacturonic acid residues. Although this group did not find rhamnose, another group did find rhamnose recently in isolated G-layers (Nishikubo et al., 2007).
In a recent gene-expression study on Populus tension wood, a member of the family 4 RG I hydrolases was upregulated (Andersson-Gunnerås et al., 2006). This upregulation is of interest for two reasons. First, because the presence of arabinan side-chains inhibits the cleavage of RG I by RG I hydrolases (McDonough et al., 2004), RG I hydrolase in the G-layer would only degrade de-branched RG I molecules. Therefore, the G-layer would tend to become enriched in highly branched RG I molecules through the removal of de-branched RG I by RG I hydrolases. Secondly, it would seem counterproductive for trees to produce hydrolases for polysaccharides that are not present. Therefore, if RG I hydrolases are produced in tension wood, it seems logical to assume that RG I is probably present at some point.
One question that remains is: why has the presence of this polysaccharide in the G-layer not been more frequently reported The fact that RG I and AGP are present in the G-layer of both sweetgum and hackberry, two unrelated tree species, indicates that these polysaccharides are likely to be normal components of the G-layer of other angiosperm trees as well. Maybe certain pectins are lost during the isolation of G-layers, perhaps by the sonication used in previous studies to isolate G-layers from tension wood sections (Norberg and Meier, 1966; Furuya, 1970; Nishikubo et al., 2007).
Xyloglucan in tension wood
Xyloglucan was recently reported by Nishikubo et al. (2007) to be the most abundant noncellulosic polysaccharide component of the G-layer. Using the same antibody for fucosylated xyloglucan, CCRC-M1, however, we found very little, if any, CCRC-M1-reactive xyloglucan in the G-layer of sweetgum. Interestingly, Nishikubo et al. (2007) showed substantial labeling of the G-layer of fibers from trees that were grown in a greenhouse and then tipped at an angle for 2 months, but in field grown trees they found very little CCRC-M1-reactive material in these G-layers. In fact, the CCRC-M1 labeling pattern shown here for sweetgum looks very similar to the labeling they showed on these older, field-grown trees. Additionally, another antixyloglucan antibody, LM15 (for nonfucosylated xyloglucan), was found to label primarily the vessels and, to a lesser extent, the walls of normal wood cells. This antibody had only a very minor reaction with the walls of G-fibers (Fig. 3B), demonstrating the fact that the pattern of CCRC-M1 labeling is not just reflecting the de-fucosylation of xyloglucan in the G-layer.
Normal wood vs. tension wood
As noted earlier, the middle lamella appears to be thinner between G-fibers and thicker in the normal wood. The thinner middle lamella may be required to prevent the G-fiber cells from sliding past each other or physically compressing under the enormous stress from the weight of the tree/branch. Although not actually in the G-layer, JIM13-reactive AGPs are present in increased concentration in the other layers of the walls of G-fibers, consistent with reports of increased AGP gene expression in tension wood (Andresson-Gunneras et al., 2006). There also appears to be an increase in the amount of xylan in the secondary walls of G-fibers as opposed to normal wood cell walls. There is a nearly complete lack of RG I (i.e., there is very little CCRC-M7, -M10, -M34, and -M22 labeling) and AGP (no JIM14 labeling) in the walls of normal wood cells. CCRC-M22, alone, appears to label the walls of normal wood cells in any quantity. It would seem, then, that a very low "baseline" level of RG I is present in the walls of most wood cells. During induction of the G-layer, the production of CCRC-M22-reactive RG I molecules increases (as reflected by the increase in CCRC-M22 binding) and either AG side-chains or free AG/AGP is also synthesized (appearance of CCRC-M10, -M7, -M34, and JIM14 signals).
Possible role of AG/AGP/RG I in the G-layer
Norberg and Meier (1966) reported a dramatic lateral shrinking of isolated G-layers of up to 25% of their initial diameters upon drying. Their conclusion was that this shrinkage was indicative of a highly porous nature of the wall, with many water-filled interstices or "capillaries" between the cellulose microfibrils. Similarly, Clair and Thibaut (2001) used scanning electron microscopy and atomic force microscopy on blocks and sections of tension wood to show that the G-layer shrinks significantly upon drying, with the conclusion that there must be a "hygro-sensible" zone within the cellulose microfibrils.
Arabidopsis seed coat mucilage (RG I) swells macroscopically upon hydration to hold water for the use of the seed and embryo (Penfield et al., 2001; Haughn and Chaudhury, 2005). AGPs have also been reported to have a water-holding capacity in several different organisms (Vicre et al., 1998; Kremer et al., 2004). Additionally, CCRC-M7-reactive polysaccharides (possibly very similar to those found in the G-layer in the current study) were preferentially associated with the water-conducting cells of bryophytes (Ligrone et al., 2002). Thus, the results of the current study seem to indicate that the hydration-sensitive wall component posited by these (and other) researchers may in fact be a highly hydrophilic RG I/AG/AGP material. As the moisture level of the G-layer decreases, this RG I/AG/AGP material would shrink and exert a pulling force on the extended cellulose microfibrils, thus generating a longitudinal stress. The shrinking of this RG I/AG/AGP material would seem to be a more likely source of the tension that has previously been ascribed to cellulose crystallites (Bamber, 2001) and noncrystalline cellulose or hemicellulose (Clair et al., 2006). Further study will be required to determine the exact role of these polysaccharides in the G-layer.
Possible practical applications of these findings
Currently, researchers are beginning to use model systems such as poplar to genetically engineer trees with properties that are better suited to human use. Thus, the discovery that the force generated by tension wood comes not from cellulose (which cannot be removed from wood) but rather from a separate polysaccharide (or polysaccharides), means these genes could be potentially removed or their expression could be altered to yield a tree that cannot produce tension wood and thus would generate ideal lumber.
Alternatively, it may be possible to treat nondried lumber that contains tension wood with enzymes that selectively degrade these polysaccharides, and thus prevent warping during drying. This enzyme treatment might allow more of a tree, such as large branches or bent trees, etc., or trees which would have been discarded to be converted into lumber, thus lowering the cost of lumber or at least reducing the number of trees required for a given amount of lumber.
Conclusion
The G-layer has long been thought to be composed of nearly pure cellulose (Norberg and Meier, 1966). By using newly available antipolysaccharide antibodies, we found evidence for the presence of RG I, AG, and AGP in the G-layer of sweetgum and hackberry. The G-layer does not appear to contain significant quantities of HG or XG. Our results support previous reports that suggested that AGPs were present in tension wood. Furthermore, both the acidic nature of the G-layer, as evidenced by toluidine blue staining, and the binding of the G-layer by several antibodies thought to specific for RG I are evidence that the G-layer is likely to contain RG I in addition to AGP. The presence of RG I in the G-layer is especially interesting because RG I is the major component of seed coat mucilage in Arabidopsis, which swells macroscopically when in contact with water. Because of this dramatic swelling associated with RG I, the tension created by G-fibers is likely derived from the pectin component of the G-layer, rather than from cellulose.
FOOTNOTES
1 The authors acknowledge the expert assistance of D. and O. Bowling in collecting specimens for this study and technical assistance of B. Maxwell. Development and distribution of the CCRC-series antibodies were supported in part by NSF grants DBI-0421683 and RCN-0090281. J. P. Knox provided samples of LM15 monoclonal antibody. A.B. was supported by a headquarters-funded Research Associate Program grant to K.V. Mention of a trademark, vendor, or proprietary product does not constitute an endorsement by USDA. 
2 Author for correspondence (e-mail: Kevin.Vaughn{at}ars.usda.gov)
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