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First published online May 22, 2003; 10.1104/pp.103.021873 Plant Physiology 132:1033-1040 (2003) © 2003 American Society of Plant Biologists Tensile Properties of Arabidopsis Cell Walls Depend on Both a Xyloglucan Cross-Linked Microfibrillar Network and Rhamnogalacturonan II-Borate Complexes1Department of Food Materials Science, Institute of Food Research, Norwich Research Park, Colney, Norwich NR4 7UA, United Kingdom (P.R., A.C.S.); Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Colney, Norwich NR4 7UH, United Kingdom (K.S.-S., K.F., M.C.M.); and Department of Molecular and Cell Biology, 75 North Eagleville Road, University of Connecticut, Storrs, Connecticut 062693125 (W.-D.R.)
The mechanical properties of plant organs depend upon anatomical structure, cell-cell adhesion, cell turgidity, and the mechanical properties of their cell walls. By testing the mechanical responses of Arabidopsis mutants, it is possible to deduce the contribution that polymers of the cell wall make to organ strength. We developed a method to measure the tensile parameters of the expanded regions of turgid or plasmolyzed dark-grown Arabidopsis hypocotyls and applied it to the fucose biosynthesis mutant mur1, the xyloglucan glycosyltransferase mutants mur2 and mur3, and the katanin mutant bot1. Hypocotyls from plants grown in the presence of increasing concentrations of dichlorobenzonitrile, an inhibitor of cellulose synthesis, were considerably weakened, indicating the validity of our approach. In order of decreasing strength, the hypocotyls of mur2 > bot1 and mur1 > mur3 were each found to have reduced strength and a proportionate reduction in modulus compared with wild type. The tensile properties of the hypocotyls and of the inflorescence stems of mur1 were rescued by growth in the presence of high concentrations of borate, which is known to cross-link the pectic component rhamnogalacturonan II. From comparison of the mechanical responses of mur2 and mur3, we deduce that galactose-containing side chains of xyloglucan make a major contribution to overall wall strength, whereas xyloglucan fucosylation plays a comparatively minor role. We conclude that borate-complexed rhamnogalacturonan II and galactosylated xyloglucan contribute to the tensile strength of cell walls.
Cell walls constrain the rate of plant cell expansion during growth and limit the final size that plant cells achieve by resisting tensile stresses generated within the wall as a consequence of turgor pressure within the cell (Carpita, 1985  ; Cosgrove, 2000; Darley et al., 2001). There are two major polysaccharidic structural networks in the walls of dicotyledonous plants: the cellulose network tethered by cross-linking glycans and the pectin network (McCann and Roberts, 1991; Carpita and Gibeaut, 1993). The cellulose network dominates the mechanical response of isolated cell walls in small deformation rheology measurements (Whitney et al., 1999), but the manner in which the cellulose is deposited is conditioned by the presence of other molecules, leading to gross mechanical differences (Whitney et al., 1995, 1999; Chanliaud and Gidley, 1999; Chanliaud et al., 2002). In work with onion (Allium cepa), a non-graminaceous monocot with a cell wall composition typical of a dicotyledon (Redgwell and Selvendran, 1986), Wilson et al. (2000) obtained evidence for the independence of the cellulose and pectin networks in the epidermis and showed that pectin is mechanically important in its own right as well as affecting the viscoelastic properties of the cell wall through its modification of cellulose hydration. However, the specific structural features of cell wall polysaccharides that influence mechanical properties have not been identified.
The cellular structure of plants can be modeled as a liquid-filled foam (Gibson and Ashby, 1996
The availability of Arabidopsis mutants with cell wall phenotypes allows us to determine the contributions that individual polymers might make to the mechanical properties of plant organs. Arabidopsis inflorescence stems have been used previously for the measurement of mechanical phenotypes, appropriately so for mutants related to secondary wall formation (Turner and Somerville, 1997
In the case of the Fuc biosynthesis mutant mur1, the mature plant is dwarfed and requires about one-half the tensile force as wild type to break elongating inflorescence stems (Reiter et al., 1993
In this paper, we describe a method to measure the mechanical behavior of portions of dark-grown hypocotyls to define the contributions of specific cell wall polymers as load-bearing elements of cell walls. Arabidopsis stems have been tested in tension (Reiter et al., 1993
In this paper, we examine the consequences of modifications to the cellulose-xyloglucan network and borate cross-linked RG II dimers. Cellulose content was titrated by growing hypocotyls in the presence of various concentrations of 2,6-dichlorobenzonitrile (DCB), whereas xyloglucan structure was modified in the cell wall mutants mur1, 2, and 3. mur1 lacks Fuc in all aerial portions of the plant because of a defect in the de novo synthesis of GDP-L-Fuc. mur2 is impaired in a xyloglucan-specific fucosyl transferase (Vanzin et al., 2002
Development and Validation of the Method Intact seedlings were mounted with cyanoacrylate glue across two aluminum tabs held in a transfer clamp 3 mm apart to select regions along the hypocotyl. During the tensile test, the plantlet was submerged in liquid medium to maintain turgor. A force displacement curve for a wild-type hypocotyl is shown in Figure 1A. Strain is the ratio of change in length to the original length and is dimensionless. Stress is the force per unit of cross-sectional area (megapascals). Two tensile parameters are defined at failure; the maximum strain is termed the failure strain, the maximum stress is the tensile strength. The ratio of stress to strain varies during the tensile test. The tensile modulus (megapascals) is defined as the ratio of stress to strain at the point where the slope of the force displacement curve is at a maximum and linear.
The greatest variation in mechanical properties within the length of the hypocotyl is that between expanded and expanding zones, as shown by the measurement of strain distribution over the full length of the hypocotyl (Fig. 1B). The dark-grown wild-type hypocotyl at 4 d has an average length of 10.2 ± 1.3 mm. The apical quarter is tapering and extremely fragile, so tensile tests must avoid this region. The basal 6 mm is cylindrical and has an average diameter of 0.24 ± 0.03 mm. Within this region, lower portions were on average 12% stronger (P < 0.05) than upper portions (Fig. 1C), whereas moduli and failure strains did not differ significantly. This lowest erect portion of the hypocotyl, in which the cells are fully expanded by d 3 and are of approximately uniform length (Gendreau et al., 1997
To establish the range over which mechanical properties can be measured, populations of hypocotyls were grown in the presence of DCB to inhibit the synthesis of cellulose, the major load-bearing polymer in the wall. Radiolabeled Glc incorporation into acetic-nitric acid-insoluble material (Updegraff, 1969
As an example of a mutant with a known mechanical phenotype, bot1-1 hypocotyls were assayed. The alleles bot1 and fra2 have a mutation in the same gene, AtKSS, which encodes katanin p60, a microtubule severing protein (Bichet et al., 2001
Xyloglucans can hydrogen bond to cellulose microfibrils to form networks and are hypothesized to be load bearing in the wall (Passioura and Fry, 1992
The large differences in mechanical phenotypes among the mur mutants could arise from differences in structural features other than cell wall composition. First, we measured hypocotyl strength in the absence of turgor. Turgor is essential to the rigidity of a primary tissue. Plasmolyzed hypocotyls have no resistance to bending, and the effect of turgor on tensile properties may be considerable. Hypocotyls of the wild type and the mur mutant with the most extreme phenotype, mur3-1, were plasmolyzed in mannitol and then tested in tension. Greater differences were observed in strength and modulus of the flaccid hypocotyls than the turgid hypocotyls (Fig. 2B), differences that were highly significant (P < 0.001). Second, we verified that the mutants did not have aberrant anatomical phenotypes or wall thicknesses. Hypocotyls of wild type, mur1-1, mur2-1, and mur3-1 were cryofixed and fractured in the FESEM for analysis of tissue anatomy (Fig. 2C) and measurements of the inner and outer epidermal walls. mur2-1 and mur3-1 were very similar to wild type. The cells of the endodermis of mur1-1 were less expanded in the radial direction than in wild type, although all of the other cells appeared normal. The radial widths of the endodermal cells in six fractured hypocotyls were as follows: wild type, 15.6 ± 3.4 µm; mur1-1, 13.4 ± 4.1 µm; mur2-1, 15.8 ± 3.6 µm; and mur3-1, 16.0 ± 4.1 µm. Only mur1-1 was significantly different from wild type (Dunnett's, P < 0.05). Cell wall thicknesses were variable but not significantly different between wild type and the three mur mutants (data not shown). Third, we verified that the mode of failure was by cell breakage rather than loss of cell-cell adhesion. Wild-type and mur3-1 hypocotyls broken in a tensile test showed no evidence of cell separation at the fracture surface (Fig. 2D). Therefore, we can assume that the mechanical properties of the cell walls will contribute more to the mechanical properties of the organ than domains of cell-cell adhesion between cells, the pectin-rich middle lamella.
In mur1-1, the mature leaf is dwarfed and only 56% of its RG II is dimerized, compared with 95% in wild type. By watering with boric acid, the growth phenotype of the mur1 rosette can be rescued and the proportion of RG II that is dimerized increases to 78% (O'Neill et al., 2001
Strength and modulus scale similarly in the mur mutants as in the DCB-treated hypocotyls and bot1-1, and there are no significant differences in failure strains. However, the mur mutants exhibit considerable reductions in strength and modulus for rather slight changes in diameter, which are shown in Figure 4. The modulus and strength of bot1-1 is similar to that of mur1-1, but its diameter is much greater.
Testing of the pedicel allows an organ of equivalent dimensions to the hypocotyl but with a greater extent of secondary wall formation to be examined. When the silique was 3 mm long, specimens of wild-type pedicels had a mean diameter of 0.24 ± 0.01 mm, a tested length of 3.17 ± 0.37 mm, and a similar mean modulus, 26.55 ± 4.83 MPa. The strength was about twice as high as that of the hypocotyls, 2.24 ± 0.27 MPa, and the failure strain was much greater, 0.35 ± 0.10. The modulus, strength, and failure strain of wild type, mur2-1, and mur3-1 did not differ significantly (Fig. 5). The pedicels of mur1-1 and mur1-2 had a strength and failure strain about one-half that of wild type (P < 0.001 and P < 0.001), but there was no significant difference in modulus.
The hypocotyl has a simple and consistent anatomy in which all growth is a consequence of cell expansion without division (Gendreau et al., 1997 ). Although DCB treatment and the bot1-1 mutation induced radial swelling, the three mur mutants had a reasonably consistent anatomical structure, wall thickness, and diameter. Thus, we have accounted for the two parameters in the foam model of porosity and edge/face distribution of material. We also used FESEM to demonstrate that the mode of failure involves fracture across cells rather than differences in cell-cell adhesion. Finally, we showed that, although turgor pressure makes a significant contribution to organ mechanical properties, the differences between wild type and mutant can be observed in its absence, i.e. in plasmolyzed tissues. We conclude that differences in organ strength can be reasonably interpreted as a consequence of the changes to the composition of the matrix of the foam, i.e. the cell walls. DCB-treated hypocotyls with decreased cellulose content showed correspondingly decreasing tensile strength and modulus. The bot1-1 mutant is already known to be mechanically weaker, and we established that this phenotype could also be measured in hypocotyls. Thus, we used DCB treatment and a known mutant to establish that our tensile test would be sensitive to compositional and mechanical changes in hypocotyls, themselves already fragile.
Artificial constructs of bacterial cellulose and plant hemicellulose (Whitney et al., 1999
mur1 has less than 2% of the normal amounts of Fuc in aerial parts of the plant (Reiter et al., 1997
Plant Material and Growth Conditions Seeds of Arabidopsis (Col-0) and mutants in the Col-0 background were surface sterilized in a mixture of 3% (v/v) hydrogen peroxide and 50% (v/v) ethanol for 2 min. After rinsing in sterilized water, seeds were plated on a nutrient-solidified medium (0.44% [w/v] Murashige and Skoog [Duchefa, Haarlem, The Netherlands], 1% [w/v] Suc, and 0.5% [w/v] Gellan gum [Phytagel, Sigma, Gillingham, Dorset, UK] at pH 5.5). Some plates were supplemented with DCB at up to 0.5 µM, and others with 1.2, 2.5, and 4.9 mM boric acid. Medium (Murashige and Skoog recipe) was prepared without borate salts and using Analar water for experiments using borate-free plates. Plates were sealed with laboratory film and placed horizontally in the dark at 25°C for 2 d, exposed to light for 4 h, and then left in the dark for 4 to 10 d. Seeds of Col-0, mur1-1, mur1-2, mur2-1, and mur3-1 were obtained from the Arabidopsis Biological Resource Center (Ohio State University, Columbus), and botero1-1 was kindly supplied by Dr Herman Höfte (Institut National de la Recherche Agronomique, Versailles, France).
Two wild-type hypocotyls were glued at their extremities to a small stretching device. The hypocotyls were wetted and sprinkled with coal dust. Strain was applied slowly in increments. The hypocotyls were imaged (Image Pro, Media Cybernetics, Silver Spring, MD, at 40x magnification), and the strains in quarter portions of the hypocotyls were measured.
At 4 d, wild-type hypocotyls were 11 mm high. Hypocotyls turned erect within 1 mm of the root boundary. Whole plants were fixed with cyanoacrylate (Resist H20, Holdtite, Gateshead, UK) across two aluminum tabs held in a brass transfer clamp about 3 mm apart. The adhesive was cured rapidly with 20 µL of an activator (Cyanolit Plus, Eurobond, Sittingbourne, UK). The glued specimens were submerged in liquid Murashige and Skoog medium + 1% (w/v) Suc, and the section of the hypocotyl between the aluminum tabs was imaged using a microscope (Image-Pro, Media Cybernetics), and the length of the specimen and 10 diameters were measured. Specimens were tested in tension submerged in the same medium using a TA-XT2i texture analyzer (Stable Microsystems, Godalming, Surrey, UK) with a load cell sensitive to 1 mN. Hypocotyls were also plasmolyzed in a 0.4 M mannitol-supplemented liquid Murashige and Skoog-Suc medium (Wu et al., 2000
During the polymerization of the cyanoacrylate, an elastic strain of up to 4% can develop in the specimens; therefore, specimens were first relaxed by lowering the crosshead by 0.1 mm at 0.03 mm s-1, and then they were extended at 0.03 mm s-1 until failure (Fig. 1A). From the force displacement curve, the maximum slope, the decrease in force on breaking, the extension on breaking, and the slack length were recorded (Cleland, 1967
Statistical comparisons, either Dunnett's or Tukey's tests, used the loge transformations (Minitab, 1994
Pedicels were taken with siliques 3 mm long from near the apex of the main inflorescence stems of 41- to 48-d-old plants. Whole pedicels were glued across the aluminum tabs to test the segment between 1 mm from the silique and 2 mm from the stem and imaged. Pedicels were tested in tension in air at an extension rate of 0.05 mm s-1, and strengths were calculated as for the hypocotyls. Breaking forces of inflorescence stems were determined as described by Reiter et al. (1993
Hypocotyls were frozen by plunging into liquid nitrogen slush at -210°C and then fractured in the SEM (Burton et al., 2000 ). The SEM micrographs were taken at 5 kV or below using an XL30 FESEM (Philips, Eindhoven, The Netherlands) fitted with a CT1500HF cryo-system (Oxford Instruments Abingdon, Oxford, UK). Samples were routinely sputter coated with 2 to 4 nm of platinum before imaging. Measurements of cell size and epidermal cell wall thicknesses were made directly on samples in the microscope using the Philips imaging software. Between five and 10 individuals were measured for each mutant line and the wild type.
Upon request, all novel materials described in this publication will be made available in a timely manner for noncommercial research purposes, subject to the requisite permission from any third party owners of all or parts of the material. Obtaining any permissions will be the responsibility of the requestor.
We thank Julia Corsar and Nicola Stacey for growth of materials and Sue Bunnewell for media preparation. We are grateful to Nick Carpita and Keith Roberts for helpful discussions. Received February 17, 2003; returned for revision March 18, 2003; accepted March 18, 2003.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.021873.
1 This work was supported by the Biotechnology and Biological Sciences Research Council (competitive strategic grants to P.R., A.C.S., and M.C.M.), by a Royal Society University Research Fellowship (to M.C.M.), by the U.S. Department of Energy (grant to W.-D.R.), and by the National Science Foundation (grant to W.-D.R.).
2 Present address: Department of Biological Sciences, Purdue University, West Lafayette, IN 47907–1392. * Corresponding author; e-mail andrew.smith{at}bbsrc.ac.uk; fax 44–1603–507723.
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, first (basal); 
, second; 
, third; and 
, fourth (apical) portions of two 4-d-old wild-type hypocotyls in which a strain was applied across the whole length of the hypocotyl. At the next increment, both had broken. C to E, Tensile properties of hypocotyls showing average strength and average modulus ± one SD (n = 20). C, Sections (2.5–2.8 mm) were tested from the lowest erect portion of 4-d-old wild-type hypocotyls (
). Lower parts of 10-d-old dark-grown wild-type hypocotyls (
), or 0.25 (
) compared with wild type (
, 5 mM boric acid. A, Black symbols, mur1-1; B, white symbols, Col-0.
-L-Galp residues (O'Neill et al., 2001
