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Physiology and Biochemistry |
2Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824 USA; 3W. J. Beal Botanical Garden, Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824 USA
Received for publication April 3, 2006. Accepted for publication June 21, 2006.
ABSTRACT
Wood, or secondary xylem, is composed mostly of three components—cellulose, hemicelluloses, and lignin. Yet this apparent simplicity is deceiving because the sophisticated arrangement of the components on various structural levels, ranging from intricate molecular architecture to defined cellular arrangements to tissue morphology, makes wood a challenging and interesting subject of biomechanical investigation. Recent advances in genetic transformation, providing easier access to wood of specifically altered composition or structure, have opened new opportunities for research on the intricate relation between material structure and composition and mechanical properties. At the same time, investigations into the mechanical properties have provided new information regarding the structural configuration of wood. The present paper reviews the work conducted in this field and outlines future perspectives and prospects for research.
Key Words: cell wall • cellulose • genetics • hemicellulose • lignin • modulus of elasticity • stiffness • viscoelasticity
Wood, or secondary xylem, is a water-conductive and supportive vascular tissue characteristic of most trees. Wood is mainly composed of tracheary elements providing water conduction and fibers providing mechanical integrity, along with parenchymatous cells adapted for storage functions. Although wood formation is an evident characteristic of trees and elaborate processes such as the formation of tension or compression wood are restricted to trees, many herbaceous plants, including Arabidopsis thaliana and tobacco (Nicotiana tabacum), develop a vascular cambium and form secondary xylem. These plants can thus be considered to a certain extent as model organisms to study xylogenesis and wood properties (reviewed by Nieminen et al., 2004
). Because routine procedures for genetic transformation of trees only recently have become well established, references to work on Arabidopsis and tobacco are included in the present paper.
The emphasis of selective tree breeding programs in the past was placed on increasing volume and yield, whereas little attention was given to changing the mechanical properties of wood (Senft et al., 1985
). As a result, the wood produced by faster growing trees tended to be inadequate for use as dimensional lumber, thus requiring subsequent refining for use in oriented strand board and particle board products.
In recent years, the rapidly increasing knowledge of plant genomes has raised the possibility of genetically manipulating trees and other woody plants at a rate faster than that afforded by traditional tree breeding programs. Advancements in gene cloning and genomics technology in forest trees have fostered the introduction of value-added traits for wood quality and for resistance to biotic and abiotic stresses into genotypes, adding a new dimension to forest tree improvement programs (reviewed by Merkle and Nairn, 2005
; Nehra et al., 2005
). With mechanical versatility being one of the defining advantages of wood as a material for engineering and construction, a clearer understanding of wood and tree biomechanics will be both of crucial importance and a potential blueprint for future genetic transformation of trees.
The genome of poplar has been mapped completely, and extensive expressed sequence tag (EST) databases cataloging the kinds of genes and their expression levels in a particular tissue are readily available for Pinus, Picea, Populus, and Eucalyptus (e.g., GenBank, NCBI). Various studies on xylem tissue have involved specifically tailored gene expressions, manipulating the composition, amount and/or structural arrangement of individual cell wall components (e.g., Huntley et al., 2003
; Zhong et al., 2003
; Joshi et al., 2004
).
The current challenge lies not in finding the gene targets and manipulating their expression, but in understanding how the genetic alterations impact the mechanical properties of the living tree and the wood products derived from it. Research in this area—the biomechanics of transgenic wood—will not only enable us to increase the economic value of wood by improving specific traits such as increased strength, controlling the formation of reaction wood or the ease of fiber separation for pulping, but it also harbors the potential for answering fundamental questions of structural arrangement of cell wall components (Hepworth et al., 1998
; Laborie et al., 2004
) and their interactions in defining the bulk mechanical properties (Hepworth and Vincent, 1998
; Zhong et al., 2005
). From a technical perspective, these objectives will benefit from efficient methods for multiple-gene transformation that enable the simultaneous modifications of multiple cell-wall traits (Chabannes et al., 2001a
; Abbott et al., 2002
; Li et al., 2003
).
Traditional studies investigating the mechanical impact of individual cell wall features had to rely on comparing different species (e.g., Köhler, 2000
) or different growth habitats (e.g., Chabbert et al., 1997
). Results from such studies are prone to remain inconclusive due to the multitude of simultaneous variations in terms of tissue and cell wall structure (e.g., Hoffmann et al., 2003
). These obstacles are overcome by the transgenic approach providing plant material of specifically taylored, restricted, and well-defined alteration in cell wall composition and structure.
LIGNIN
Efforts to alter wood have mainly focused on lignin, the second most abundant component of wood, primarily because of the economic importance of lignin removal during pulping and because lignification is a remarkably flexible process amenable to genetic alterations. From a mechanical perspective, lignin is the main load-bearing element of the wall matrix and therefore of pivotal importance for the mechanical properties of the wood (Jeronimidis, 1980
). While the importance of investigating the biomechanical consequences of lignin alteration is recognized even outside the field of biomechanics (Anterola and Lewis, 2002
), biomechanical studies on transgenic trees with altered lignin are still scarce. Many excellent reviews have considered the details of the lignin biosynthetic pathway and the impact of genetic engineering of that pathway on the biogenesis of lignins (Mellerowicz et al., 2001
; Anterola and Lewis, 2002
; Humphreys and Chapple, 2002
; Boerjan et al., 2003
), emerging models for metabolic feedback control of lignification (Blee et al., 2003
), and factors that control where and when the lignin biosynthetic pathway is invoked (Rogers and Campbell, 2004
).
The lignification of xylem is an adaptive trait of great significance. A conserved regulatory network of monolignol genes that are involved in the synthesis of guaiacyl lignin in xylem suggests that these genes were highly conserved during evolution (Raes et al., 2003
). Molecular evolution and comparative functional studies support the hypothesis that genes leading to the biosynthesis of syringyl lignin in the fiber cells of angiosperms evolved more recently (Peter and Neale, 2004
).
Lignin not only defines the mechanical properties of wood, but also impacts water transport in terms of vulnerability of vessels to implosion (Franke et al., 2002
; Jacobsen et al., 2005
). Recent findings indicate that a tree's response to growth conditions, including leaning or bending of the stem, is not restricted to changes in tissue morphology but includes changes in lignin composition and in the pattern of its deposition in different cell types (Chen et al., 2000
; Pruyn et al., 2000
; Yoshida et al., 2002
). Results from work on transgenic tobacco lines indicate that the spatial pattern of lignin deposition is tightly and independently regulated in individual cell types and cell wall sublayers (Chabannes et al., 2001b
). The monomeric composition of lignin varied not only across different plant species, but also according to the individual requirements of lignin properties in different cell types (Yoshinaga et al., 1992
) and in response to environmental conditions (e.g., Chabbert et al., 1997
; Donaldson, 2002
). Lignification therefore can be seen as a remarkably versatile tool allowing plants considerable flexibility in dealing with environmental stresses as diverse as mechanical challenges, drought, or pathogens.
The structure of natural lignin polymers is complex: the molar mass, charge density, degree of branching, cross-link density, and the type of inter-unit linkages are widely changeable. Accordingly, there is a wealth of possible lignin alterations with impact on immediate biomechanical features such as modulus of elasticity, stress–strain characteristics, and viscoelastic damping and the vulnerability to embolism and allometry. Until now, only basic characteristics of lignin-modified wood such as the modulus of elasticity or bending stiffness have been evaluated. A summary of modifications in lignin amount and composition and impact on biomechanics is shown in Table 1.
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found a decrease in work of fracture (0.026 vs. 0.037 nJ/mm2) in wood from poplars downregulated in the activity of caffeic acid/5-hydroxyferulic acid O-methyltransferase (COMT). COMT is an enzyme in the lignin biosynthetic pathway required primarily for syringyl (Humphreys and Chapple, 2002
).
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; Köhler, 2000
; Burgert et al., 2004
), and optimizing for multiple requirements such as mechanical integrity and water conduction (Kern et al., 2005
). A more detailed discussion of the influence of lignin on micromechanical processes can be found in the studies by Hepworth and Vincent (1998)
, Köhler and Spatz (2002)
, and Keckes and co-workers (2003)
. The lower tolerable limit of lignin concentration is obviously defined by the onset of general cell wall disorganization (Turner and Somerville, 1997
; Chabannes et al., 2001b
; Jones et al., 2001
), indicating that a minimum amount of lignin is needed for anchoring the cellulose and hemicellulose components together for proper cell wall genesis and maintenance of structural integrity.
Lignin composition
The mechanical effects of altering the monomeric composition of lignin are less obvious than changing total content and have received little attention. Manipulating the expression of ferulate 5-hydroxylase (F5H) provides compelling evidence that plants have considerable malleability regarding lignin monomer composition. F5H acts further downstream in the lignin synthesis pathway, converting 5-hydroxy-coniferylaldehyde and 5-hydroxyconiferylalcohol towards the synthesis of sinapyl alcohol, i.e., syringyl. Although wildtype plants produce a rather narrow range of syringyl (S) to guaiacyl (G), plants are capable of sustaining considerable variation, with guaiacyl contents ranging from 3 to 100% (Ralph et al., 2004
). Lignin monomer composition differs for different cell types and growth conditions, suggesting involvement in the adjustment of cells to specific requirements. It is instructive to consider the biomechanical impact of altering the S : G ratio.
Our work on F5H-modified poplar (P. tremula x P. alba) demonstrates a gradual rise of the elastic modulus upon progressive increase of syringyl, with an increase of 37% when raising S : G by 25%. Despite statistically significant increases in elastic modulus, bending stiffness remains unchanged across the transgenic strains. The increased modulus is compensated by a reduced stem diameter. This indicates feedback between the mechanical properties of the wood and material allocation. No undesirable pleiotropic side effects or tissue alterations were detectable (Huntley et al., 2003
).
With the C5 position methoxylated, syringyl offers less opportunity for polymer interlinkages then guaiacyl, and it seems the more linear architectural patterning of syringyl lignin, due to the predominant endwise polymerization (ß-O-4-coupling; for a review, see Ralph et al., 2004
), favors a closer packing of the lignin within the cell wall, which in turn leads to increased stiffness. As discussed by Goring (1988)
in view of a modified paradigm for structure and randomness of the lignin polymer, there are substantial space restrictions for lignin in the secondary cell wall, limiting the lignin polymer to a mirror image on a molecular scale of the narrow lamellar ultrastructure of the cellulose microfibrils. Our preliminary x-ray density measurements support this view, showing higher wood density in the F5H over expressing transgenic poplars.
As evident from UV-microspectrophotometric measurements comparing light absorption at 273 nm for syringyl to that at 280 nm for guaiacyl (Musha and Goring, 1975
), the typical pattern of differences in lignin monomer composition between different cell types is conserved in the mutant, showing higher relative guaiacyl content in vessel walls and higher syringyl content in fibers (Fig. 2). Despite the genetically shifted S : G ratio, the plant maintains relative differences in S : G according to cell type and function. Considering the bearing of syringyl content on the elastic modulus shown by our study, the conserved pattern of lignin composition according to cell type could be a hint to the importance of a gradient in the mechanical properties between vessel and fiber walls (compare Suresh, 2001
; Jacobsen et al., 2005
).
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Considering the substantial alterations entailed by the addition of a metoxy group to the monomer unit as discussed previously for the F5H transgenic poplars, a sizable potential of tailoring wood mechanical properties through genetic lignin modification can be expected. Along with novel measuring techniques, such as neutron scattering to study structural and dynamical properties at different relevant length scales (Arbe et al., 2001
; Lairez, 2005
), and in combination with molecular modeling, biomechanical investigations will further advance our understanding of the complex structural configuration of wood.
STRUCTURAL CARBOHYDRATES
Cellulose and hemicelluloses constitute the main load-bearing structural elements in the secondary cell walls of xylem. Cellulose is an unbranched polymer of ß-1,4-linked glucose residues. While the chemical structure is intriguingly simple, structure and quantity of cellulose change in accordance with the biological function showing differences in the degree of polymerization, crystallinity, amount of associated polysaccharides, ratio of the crystalline allomorphs I
and Iß, and the angle of orientation of the cellulose microfibrils.
Hemicelluloses are heteroglycans, which consist of various sugar units arranged in different proportions and with different substituents. The main hemicellulosic polysaccharides found in secondary walls in dicotyledonous plants are xylans. They are composed of a backbone polymer of ß-1,4-linked d-xylosyl residues with - d-glucuronic acid or 4-O-methyl--d-glucuronic acid residues at O-2 of one of every 6–12 xylosyl residues. The xylosyl residues may also be substituted with short side chains containing l-arabinose and may be acetylated on C-2 or C-3 (Ebringerová and Heinze, 2000
; Teleman et al., 2000
).
Our understanding of cellulose synthesis and deposition is still fragmentary, and progress in this field has been slow owing to the inability to isolate active and intact cellulose synthase complexes and the intricacy of the mechanistic processes involved in the wood cellulose development (Joshi et al., 2004
). It appears that hemicelluloses are instrumental in the formation of the cellulose fibril network (Hackney et al., 1994
), and genetic alterations of hemicelluloses can both disrupt (Zhong et al., 2005
) or enhance (Park et al., 2004
) cellulose formation, with a reduction in breaking strength by 80% reported in the first case and a 20% increase in the elastic modulus reported in the latter. Cellulose and hemicelluloses also are strongly linked in the intact cell wall where glucomannan seems to be closely associated with cellulose (Salmén and Olsson, 1998
).
The overriding importance of cellulose and hemicelluloses as major structural components of the cell wall is obvious, and any decrease in cellulose content strongly affects mechanical rigidity, even if countered by a simultaneous increase in lignin (Li et al., 2003
). Yet, more sophisticated biomechanical measurements on mutants with altered cellulose and/or hemicelluloses are still rare, and mechanical measurements are mostly limited to ancillary studies in research with the main focus on other aspects.
As illustrated by the few comprehensive studies dealing with biomechanical aspects of hemicelluloses or cellulose (Hepworth and Vincent, 1998
; Åkerholm and Salmén, 2001
; Köhler and Spatz, 2002
; Fratzl et al., 2004
), there is quite a potential for shedding light on the structural configuration and coupling of cellulose and hemicelluloses and their biomechanical impact. In this context, the study by Fratzl and co-workers is particularly noteworthy, in which hemicelluloses have been suggested as acting like a natural interface polymer, comparable to proteoglycans in tendon tissue and with comparable mechanical function.
CONCLUDING REMARKS
We rely on wood for a multitude of products, as feedstock in industrial processes, and for bioenergy production. The products range from dimensional lumber and wood-based composite materials to fibers and raw chemicals. One of the key advantages of wood and wood-based composite materials is their sturdy mechanical strength even beyond the linear, elastic range of loading. Synthetic engineering materials often fail abruptly at maximum load, while wood and wood-based composites fail gradually and retain overall integrity well into the range of irreversible structural rearrangement or partial failure. As outlined in this study, genetically altered wood provides an effective tool for investigating the individual contributions of the different cell wall components to the complex mechanical properties of the wood. Selective genetic alterations to wood structure and/or composition help to clarify the mechanical role of particular wood features and also shed light on mechanisms of the trees adjusting to mechanical requirements of the environment. Therefore, research on the biomechanics of transgenic wood helps advance our understanding of the tree as a living structure and provides guidelines for silviculture and optimal exploitation of wood as a versatile natural resource and engineering material.
FOOTNOTES
1 The assistance of G. Koch (Institut für Holsforschung, University of Hamburg) with UV-microspectrophotometric measurements is gratefully acknowledged. The authors thank F. Ewers for helpful discussion. The project was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant number 2005-35103-15269. 
4 Author for correspondence (mail{at}lhkoehler.de
)
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= 272 nm and 280 nm. (B) Relative lignin composition of the same specimen as in A, calculated by comparing absorption at