Tensional stress generation in gelatinous fibres: a review and possible mechanism based on cell-wall structure and composition

Journal of Experimental Botany, Vol. 63, No. 2, pp. 551–565, 2012 doi:10.1093/jxb/err339 Advance Access publication 16 November, 2011 DARWIN REVIEW Tensional stress generation in gelatinous fibres: a review and possible mechanism based on cell-wall structure and composition Ewa J. Mellerowicz1,* and Tatyana A. Gorshkova2 1 Umeå Plant Science Center, Department of Forest Genetics and Plant Physiology, SE-90183 Umeå, Sweden Kazan Institute of Biochemistry and Biophysics, Russian Academy of Sciences, PO Box 30, Kazan 420111, Russia * To whom correspondence should be addressed. E-mail: Received 12 July 2011; Revised 28 September 2011; Accepted 3 October 2011 Abstract Gelatinous fibres are specialized fibres, distinguished by the presence of an inner, gelatinous cell-wall layer. In recent years, they have attracted increasing interest since their walls have a desirable chemical composition (low lignin, low pentosan, and high cellulose contents) for applications such as saccharification and biofuel production, and they have interesting mechanical properties, being capable of generating high tensional stress. However, the unique character of gelatinous layer has not yet been widely recognized. The first part of this review presents a model of gelatinous-fibre organization and stresses the unique character of the gelatinous layer as a separate type of cell-wall layer, different from either primary or secondary wall layers. The second part discusses major current models of tensional stress generation by these fibres and presents a novel unifying model based on recent advances in knowledge of gelatinous wall structure. Understanding this mechanism could potentially lead to novel biomimetic developments in material sciences. Occurrence of gelatinous fibres Gelatinous fibres are specialized sclerenchyma cells, characterized by their elongated shape and the presence of an inner cell-wall layer that exhibits gel-like shrinkage during drying (Clair et al., 2008), looks more or less transparent in many types of histological preparations, and hence was called ‘the gelatinous layer’. The weak interaction of this layer with most histological stains is explained by its high content of crystalline cellulose, which is not very reactive and thus remains unstained. Gelatinous fibres are found in various plant organs, including thorns, tendrils, contractile roots, corms, peduncles, and stems. They occur in phloem and xylem of both primary and secondary origin, and sometimes in non-vascular tissues (Zimmermann et al., 1968; Jourez, 1997; Tomlinson, 2003; Gorshkova and Morvan, 2006; Toghraie et al., 2006; Fisher, 2008; Bowling and Vaughn, 2009). They may form either the bulk of a tissue, as in tension wood, be grouped in bundles, or sometimes even occur singly among other plant cells. They have important functions, since they can generate high tensional stress within mature organs, thus either enabling the movement of these organs or reinforcing their structure and stability (Yoshida et al., 2002; Clair et al., 2003; Fang et al., 2008; Fisher, 2008; Abasolo et al., 2009). The best known examples of extraxylary gelatinous fibres are those in major fibre crop plants, such as flax, hemp, and ramie. Although tension has never been directly measured in such fibres, the basic wall structure, composition, and function of these cells give reason to group them together with tension wood fibres (Gorshkova and Morvan, 2006; Gorshkova et al., 2010). The efficacy of gelatinous fibres can be quite remarkable; in some plant species they can pull entire shoots underground, where they can survive adverse conditions such as freezing temperatures or fires (Fisher, 2008; Schreiber et al., 2010), and the gelatinous fibres in aerial roots of Ficus Abbreviations: MFA, microfibril angle; G-layer, gelatinous layer; S-layer, secondary layer; P-layer, primary layer; AGP, arabinogalactan protein; XET, xyloglucan-endotransglycosylase; RG I, rhamnogalacturonan I; MXE, mixed-link XET. ª The Author [2011]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: 2 552 | Mellerowicz and Gorshkova et al., 2008; Mellerowicz et al., 2008; Bowling and Vaughn, 2009). Historically, researchers attempted to apply the same model to explain both tension generation in the tension wood of angiosperms and compression generation in the compression wood of conifers (Boyd, 1985; Okuyama et al., 1994; Yamamoto, 1998; Bamber, 2001). However, although the architecture of cell walls in these two types of wood may superficially seem to represent two extremes of the same continuum – the former with low lignin contents and low cellulose microfibril angles (MFAs), and the latter with high lignin contents and high cellulose MFAs – there are major differences in the types of matrix polymer present and their organization. These differences lead to strong differences in cell-wall architecture, clearly indicating that these wood types represent very different materials and that a common model might not be applicable. Basic cell-wall structure in gelatinous fibres Tensional stress in gelatinous fibres arises from the cell-wall structure, therefore understanding the cell-wall architecture, including all the intricate interactions between the constituent polymers during their deposition and subsequent modification in muro, is essential for elucidating this physical phenomenon. The development of gelatinous fibres begins with the elongation of young fibres, which occurs either entirely (in secondary fibres) or partially (in primary fibres) by intrusive growth (between cells) (Gorshkova et al., 2011). At this stage the fibres have primary (P) cell walls and are cemented together by acidic middle lamella (Snegireva et al., 2010). During or following the final stages of elongation, successive secondary wall layers (S1, S2, to . Sn) are deposited. After formation of one to three S wall layers of varying thickness (Onaka, 1949; Araki et al., 1983), the tertiary, gelatinous layer (G) is laid down. Due to historical reasons, and the fact that S-layers are barely distinguishable in some fibres (notably flax and ramie), G-layers are sometimes referred to as parts of the secondary cell wall. However, careful observations indicate that deposition of S-layer(s) precedes that of G-layers, so an S-layer is never completely absent (Gorshkova et al., 2010); hence G-layers of cell walls are tertiary. The proportions of S- and G-layers vary widely among phloem fibres of different species: ranging from only S-layers in jute and kenaf (McDougall, 1993; Lam et al., 2003) to a high predominance of G-layers in ramie and flax (McDougall, 1993; Gorshkova et al., 2010). Interestingly, G-layers seems to be specific to fibres and are not found in other cell types (Gorshkova et al., 2010). Thus, the cell wall of a mature gelatinous fibre has layers of three distinct types: the P-layer (...truncated)