Xyloglucan: The Molecular Muscle of Trees

Abstract

Tension wood evolved in woody angiosperms to allow stems with secondary thickening to bend and thus maintain an optimal orientation. Stem bending is the result of longitudinal tensile stress that develops in tension wood tissues. In many species, a specialized secondary cell wall layer, the so-called gelatinous (G)-layer, develops, containing longitudinally orientated crystalline cellulose fibrils; these have been recently shown to generate the tensile stress by an unknown mechanism. The cellulose fibrils cannot, however, work in isolation. Both coherence between the fibrils and adherence of the G-layer to the adjacent cell wall layers are required to transfer the tensile stresses of the cellulose fibrils to the tissue. Previous work had not identified hemicelluloses within the G-layer. Sugar composition and polysaccharide linkage analyses of pure G-layers isolated by sonication have recently identified xyloglucan as the main non-cellulosic component of the G-layer. Xyloglucan has been detected by immunolabelling with the CCRC-M1 monoclonal antibody and by in-situ activity assays using XXXG–sulforhodamine substrate in the developing G-layers but not in the mature ones. However, xyloglucan endotransglucosylase/hydrolase (XTH) proteins persist in the G-layer for several years and the corresponding xyloglucan endotransglucosylase (XET) activity (EC 2·4·1·207) occurs in the adjacent layers. Correspondingly, several XTH-encoding transcripts were found to be up-regulated in developing tension wood compared with normal wood. We propose that, during cellulose crystallization, a part of the xyloglucan is trapped inside the crystal, inducing longitudinal tensile stress within it; another part of it is accessible and present between the G-layer and the outer wall layers. XET activity that occurs persistently in the G-fibres maintains coherence between the G-layer and the adjacent secondary wall layers. It is postulated that these activities are essential for generation of tensile stress during fibre maturation in tension wood.