Tensile Properties of Arabidopsis Cell Walls Depend on Both a Xyloglucan Cross-Linked Microfibrillar Network and Rhamnogalacturonan II-Borate Complexes

Abstract

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 Ͼ bot1 and mur1 Ͼ 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 galactosecontaining 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(Whitney et al., , 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...

Genetic architecture of wood properties based on association analysis and co‐expression networks in white spruce

“…In the present study, we found that genes involved in cytoskeleton development and several transcription factors were over‐represented among genes significantly associated with EW MFA. The cytoskeleton plays a key role in the establishment of cell wall ultrastructure and resulting mechanical properties of the xylem tissue (Ryden et al ., 2003; Fletcher & Mullins, 2010). These genes are involved in the two main types of cytoskeletal polymers: actin filaments and microtubules (Fletcher & Mullins, 2010).…”

The PEN1 Syntaxin Defines a Novel Cellular Compartment upon Fungal Attack and Is Required for the Timely Assembly of Papillae

“…The mur1-1 mutant has Ͻ2% of the normal amounts of fucose in aerial parts of the plant , and a tensile strength of elongating influorescences Ͻ50% that of the wild type (Bonin et al, 1997). MUR3 encodes a xyloglucan-specific galactosyl transferase (Madson et al, 2003) that considerably affects the mechanical properties of the cell wall (Ryden et al, 2003). The mur8-1 and mur10-1 mutants have complex changes in their cell wall composition .…”

Loss of Highly Branched Arabinans and Debranching of Rhamnogalacturonan I Accompany Loss of Firm Texture and Cell Separation during Prolonged Storage of Apple

“…Four complex side chains may be added in a precise configuration to form RG IIs (O'Neill et al, 1996). RG IIs may dimerize through formation of boron di-diesters, which promote normal shoot development (Ishii et al, 2001;O'Neill et al, 2001) and contributes to the tensile strength of the wall (Ryden et al, 2003). Article, publication date, and citation information can be found at www.plantphysiol.org/cgi…”

“…Four complex side chains may be added in a precise configuration to form RG IIs (O'Neill et al, 1996). RG IIs may dimerize through formation of boron di-diesters, which promote normal shoot development O'Neill et al, 2001) and contributes to the tensile strength of the wall (Ryden et al, 2003). Attached to the O-4 position of rhamnose residues of RG I are neutral sugar polymers of (1/5)-a-L-arabinans with different degrees of branching at the O-3 and O-2 positions, (1/4)-b-D-galactans, and type I arabino-(1/4)-galactans (Brett and Waldron, 1996;Willats et al, 2001).…”