Mesoporosity as a new parameter for understanding tension stress generation in trees

Journal of Experimental Botany, Vol. 60, No. 11, pp. 3023–3030, 2009 doi:10.1093/jxb/erp133 Advance Access publication 12 May, 2009 RESEARCH PAPER Mesoporosity as a new parameter for understanding tension stress generation in trees Shan-Shan Chang1,2, Bruno Clair1,*, Julien Ruelle3, Jacques Beauchêne4, Francesco Di Renzo5, Francxoise Quignard5, Guang-Jie Zhao2, Hiroyuki Yamamoto3 and Joseph Gril1 1 Received 18 November 2008; Revised 31 March 2009; Accepted 5 April 2009 Abstract The mechanism for tree orientation in angiosperms is based on the production of high tensile stress on the upper side of the inclined axis. In many species, the stress level is strongly related to the presence of a peculiar layer, called the G-layer, in the fibre cell wall. The structure of the G-layer has recently been described as a hydrogel thanks to N2 adsorption–desorption isotherms of supercritically dried samples showing a high mesoporosity (pores size from 2–50 nm). This led us to revisit the concept of the G-layer that had been, until now, only described from anatomical observation. Adsorption isotherms of both normal wood and tension wood have been measured on six tropical species. Measurements show that mesoporosity is high in tension wood with a typical thick G-layer while it is much less with a thinner G-layer, sometimes no more than normal wood. The mesoporosity of tension wood species without a G-layer is as low as in normal wood. Not depending on the amount of pores, the pore size distribution is always centred around 6–12 nm. These results suggest that, among species producing fibres with a G-layer, large structural differences of the G-layer exist between species. Key words: Growth stress, hydrogel, mesoporosity, tension wood. Introduction Tension wood (TW) is a peculiar wood tissue that is often formed in the upper side of leaning trunks and branches in hardwood species (Isebrands and Bensend, 1972) to control the orientation of the growth axis by generating high tensile stress (Wardrop, 1964; Fisher and Stevenson, 1981). For many commonly studied species such as beech, poplar, oak, or chestnut, TW is characterized by the occurrence of fibres with a particular morphology and chemical composition due to the development of the so-called gelatinous layer (Glayer). This layer is composed of cellulosic microfibrils that are nearly parallel to the fibre axis (Dadswell and Wardrop, 1955; Wardrop, 1964; Côté et al., 1969) embedded in a highly hydrated polysaccharide matrix (Nishikubo et al., 2007; Bowling and Vaughn, 2008; Mellerowicz et al., 2008). Although it has been well established that the G-layer is the driving force of the high tensile stress generated in TW (Trénard and Guéneau, 1975; Yamamoto et al., 2005; Fang et al., 2008), the underlying mechanism is still a subject of debate. In previous research, the structure of the G-layer has been described as possessing gel-like characteristics: large shrinkage (Clair and Thibaut, 2001; Fang et al., 2007) and high rigidification during drying (Clair et al., 2003). Recently, the hydrogel structure of the chestnut G-layer has been characterized thanks to nitrogen adsorption. The * To whom correspondence should be addressed: E-mail: ª The Author [2009]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: Laboratoire de Mécanique et Génie Civil (LMGC), Université Montpellier 2, CNRS, Pl. E. Bataillon, cc 048, 34095 Montpellier Cedex 5, France 2 College of Materials Science and Technology, Beijing Forestry University, Beijing, 100083, PR China 3 School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601, Japan 4 Ecologie des Forêts de Guyane (EcoFoG), CIRAD, BP 709, 97387 Kourou cedex, French Guyana 5 Institut Charles Gerhardt Montpellier,UMR 5253 Université Montpellier 2, CNRS, ENSCM, UM1, 8 rue Ecole Normale, 34296 Montpellier Cedex 5, France 3024 | Chang et al. Fig. 1. The three types of adsorption isotherms usually found by nitrogen adsorption [types I, II, and IV by IUPAC classification; reprinted from Sing et al. (1985), with kind permission from IUPAC]. P/P0: relative pressure; na/ms: quantities adsorbed g
1 sample expressed as mmol g
1. Fig. 2. Physical picture of porous solid. Reprinted from Rouquerol et al. (1999), with kind permission from Elsevier. loop is associated with the secondary process of capillary condensation, which results in the complete filling of the mesopores at P/P
<1. Pores can have a regular or, more commonly, an irregular shape, either an ink-bottle shape (pore body larger than pore mouth) or a funnel shape (the opposite). Pores can be closed (not accessible from the outside), blind (open only at one end), or through (open at both ends). Each pore can be isolated or, more frequently, connected to other pores to form a porous network (Rouquerol et al., 1999) (Fig. 2). The surface and structural properties of the pores control the interactions of material with gases, fluids, and other solids. The adsorbate desorption is the opposite of adsorption, but evaporation from mesopores usually takes place at a pressure lower than that of capillary condensation giving a hysteresis loop. The reason for the hysteresis is that the formation of the meniscus in capillary condensation is an activated phenomenon, while the retreat of the meniscus in evaporation is usually an equilibrium phenomenon. Pore shape affects the mechanisms of condensation and evaporation and four types of hysteresis have been recognized according to IUPAC classification (Sing et al., 1985) (Fig. 3). Type H1 hysteresis is characteristic of solids crossed by channels with uniform sizes and shapes. Type H2 corresponds to channels with a pore mouth smaller than the pore body (this is the case of ink-bottle-shaped pores). Type H3 chestnut G-layer contains mesopores (pore size between 2 nm and 50 nm) and the pore surface areas is more than 30 times higher than that in normal wood (NW) (Clair et al., 2008). The swelling of the G-layer matrix has been suggested recently by several authors as the possible driving force of the growth stress generation in TW (Nishikubo et al., 2007; Goswami et al., 2008). However, it is known that many species (Onaka, 1949; Fisher and Stevenson, 1981; Clair et al., 2006) are able to produce tensile stress without forming a typical G-layer. Different anatomical patterns of TW exist, from fibres with a typical G-layer to fibres exhibiting no difference at the fibre level (Clair et al., 2006; Ruelle et al., 2006, 2007). These results led us to revisit the concept of the G-layer and to propose an objective description of the TW cell wall structure, until now only defined from visual assessments (stain, detachment or swollen aspect) which are the subject of much debate (Clair et al., 2005a, b, 2006). Let us briefly introduce the principles of mesoporosity measurements by the nitrogen adsorp (...truncated)