Wood Formation in Trees

Abstract

Wood is the most important natural and endlessly renewable source of energy and therefore has a major future role as an environmentally cost-effective alternative to burning fossils fuels. The major role of wood is not only the provision of energy but also the provision of energy-sufficient material for our buildings and many other products. In addition, developing wood cells represent one of the most important sinks for excess atmospheric CO2, thereby reducing one of the major contributors to global warming. Wood is the fifth most important product of the world trade. Vast quantities of wood are logged by foresters to provide fuel, fibers (for pulp, paper products, and boards), and sawn timber (for house building and furniture) as commodities. The complex chemical makeup of wood (cellulose, hemicelluloses, lignin, and pectins) also makes it an ideal raw material for what could be a future “ligno-chemical” industry that could replace the petrochemical industry, in providing not only plastic and all kinds of chemical products, but also food and textile products. Resource analyses have led to the conclusion that wood and fiber needs over the next 40 years can only be met by logging 20% to 40% of the total present standing timber inventory in the natural forest (Food and Agriculture Organization). However, most agree that some of these forests should be either left completely alone or managed with only a minimum of wood extraction to preserve their environmental value. The solution is to try to accomplish what agriculture has been doing for the last few centuries: grow wood as a crop in the same way that we grow wheat and maize. The future of the world's forests as well as the forest products industry will therefore depend to a huge extent on our ability to domesticate wild tree species and tailor them for maximum economic yield in the highly controlled environments typical of agriculture. The domestication of forest trees must be accomplished rationally, using the best available modern scientific methods, to develop high-yielding, intensively managed plantation forests, occupying a small percentage of existing forested land. In particular, the safe and careful application of biotechnology (marker-assisted breeding, genetic engineering, and in vitro propagation) to forestry practices, should help develop genetically superior trees in a time span of only a few decades. Considering the important role that wood is foreseen to play in the near future, it is surprising to see that our understanding of how wood develops is far from complete. With a few exceptions, very little is known about the cellular, molecular, and developmental processes that underlie wood formation. Xylogenesis represents an example of cell differentiation in an exceptionally complex form. This process is controlled by a wide variety of factors both exogenous (photoperiod and temperature) and endogenous (phytohormones) and by interaction between them. It is driven by the coordinated expression of numerous structural genes (some of known function) involved in cell origination, differentiation, programmed cell death, and heartwood (HW) formation and by virtually unknown regulatory genes orchestrating this ordered developmental sequence. The presence of gene families and the extreme plasticity of the metabolism involved (as exemplified by the unusual behavior of plants with transformed cell walls; for review, see Fagard et al., 2000) add a further complexity to our understanding of the process of wood formation. The making of wood spans a broad range of topics. Rather than to attempt a detailed review of all recent works in the different fields of wood formation, it is an objective of this contribution to give a brief overview and generalized concepts of this developmental process. We first open this Update by reviewing the well-known stages leading to the formation of wood, starting from the activities in a secondary meristem (the vascular cambium) to programmed cell death via the maturation of cambial derivatives. Emphasis is made on the biosynthesis and deposition of the main cell wall compounds, as well as the mediation of this ordered developmental process by phytohormones and transcription factors. The considerable plasticity in anatomical, chemical and physical wood properties is then described in view of providing a unique opportunity to dissect the molecular and biochemical mechanisms involved in such differences. Finally, the current progress in the molecular biology of wood development is presented. Wood (secondary xylem) is manufactured by a succession of five major steps, including cell division, cell expansion (elongation and radial enlargement), cell wall thickening (involving cellulose, hemicellulose, cell wall proteins, and lignin biosynthesis and deposition), programmed cell death, and HW formation. The developmental biology of wood has been recently extensively reviewed and the following reading will provide the reader with essential references in research on vascular differentiation: Chaffey (1999), Lachaud et al. (1999), Savidge et al. (2000), Chaffey (2001), and Mellerowicz et al. (2001). The vascular cambium is a secondary meristem derived from the procambium, which in turn develops from the apical meristem (Larson, 1994). The cambium plays a major role in the diametral growth of gymnosperm and angiosperm shoots and roots and is of great significance, particularly in respect to the wood that is produced. Cambial activity ensures the perennial life of trees through the regular renewing of functional xylem and phloem. The cambial zone includes the cambium sensu stricto made up of only one layer of juvenile cells, called initials, and the phloem and xylem mother cells, which are both produced by the dividing cambial initials. A, Drawing of a transverse section of the cambial zone of maritime pine (Pinus pinaster) showing the fusiform (F) and ray (R) initial cells in the cambial zone (CZ). X, Centripetal xylem differentiation with radially enlarging, maturing, and mature xylem. P, Centrifugal phloem differentiation with radially enlarging, maturing, and mature phloem. Empty arrowhead indicates a newly deposited radial wall (anticlinal division). Full arrowhead indicates a newly deposited tangential wall (periclinal division). B, Three-dimensional scheme of maritime pine wood showing the relatively homogeneous structure of conifer xylem. Ninety percent of the wood is made of tracheids, and the remainder is composed of ray parenchyma and longitudinal parenchyma cells, as well as resin ducts in certain species. Sap water ascends via the xylem and nutritive sap descends via the phloem. Sap can also be transported radially via the ray cells and tangentially by bordered pits. It is important to note the different direction and faces which are needed to describe wood structure: transverse, radial, and tangential sections. The daughter cells, produced by the cambial initials, give rise to a wide variety of wood cells, whose unique characteristics and three-dimensional associations define the intrinsic structure of wood (Fig. 1B). In the following section we will focus on the maturation process engaged by the xylem cells: tracheids, vessels, and fibers involved in water transport and mechanical support of the entire tree. The differentiation of these cells involves four major steps: cell expansion, followed by the ordered deposition of a thick multilayered secondary cell wall, lignification, and cell death. Derivative cells expand longitudinally and radially to reach their final size during the formation of the primary wall. Xyloglucan endotransglycosylases, endoglucanases, expansins, pectin methyl esterases, and pectinases are among the primary determinants of this process. Once expansion is completed, the formation of the secondary cell wall begins, driven by the coordinated expression of numerous genes specifically involved in the biosynthesis and assembly of four major compounds: polysaccharides (cellulose, hemicelluloses), lignins, cell wall proteins and other minor soluble (stilbenes, flavonoids, tannins, and terpenoids), and insoluble (pectins and cell wall proteins) compounds in a neutral solvent (Higuchi, 1997). Between 40% and 50% of wood consists of cellulose. The fundamental structure units are the microfibrils (MFs), which are the result of a strong association of inter- and intrachain hydrogen bonds between the different chains of β-linked Glc residues in a manner so precise that microfibrillar cellulose is largely crystalline. Until recently, not even one single enzyme involved in cellulose biosynthesis and deposition was purified or cloned (Arioli et al., 2000). A first breakthrough had been the identification of genes encoding the catalytic subunit of the cellulose synthase (Ces) complex. In Arabidopsis, at least six genes encode putative catalytic subunits of Ces. In addition, a large gene family of over 20 more distantly related genes, so-called Ces-like (Csl) genes, exists, whose gene products most likely are involved in the synthesis of other polysaccharides. In higher plants, the substrate for Ces (UDP-d-Glc) is provided by Suc synthase. The complex Ces/Suc synthase is thought to have a cytoplasmic localization and the growing cellulose chain may be secreted through the membrane via a pore. Cortical microtubules (mainly composed of α- and β-tubulin) may determine the wall pattern by defining the position and orientation of cellulose MFs during the differentiation of conducting elements (Chaffey, 2000), probably by guiding the movement of the cellulose-synthesizing complex in the plasma membrane. However, although in many cases co-orientation of microtubules and MFs were observed, mathematical models (that to be in on the of the have been to this and The cellulose MFs are with of soluble the hemicelluloses, which for about of the of as such as and or as a and The biosynthesis of these polysaccharides in the by a process that can be main steps: the synthesis of the by and the of chain residues in by a variety of and The major of wood is lignin, a derived from and rise to and which from other only by their of the and to the wood as a and providing the needed for the transport of and among different cell and cell wall an units are in with biosynthesis has been the most in the of structural genes et al., et al., 2000). However, it is surprising that recent at lignin biosynthesis have that our current models of the are and wall proteins and are among the other minor compounds of the cell wall. different proteins are present in the cell wall at different during the of in the wood is such proteins could play important the and of xylem cell cell wall proteins have been in many plants and have been four main proteins, proteins, proteins, and proteins are the cell wall and probably have structural are thought to play a fundamental role in the of cell wall are also thought to be from the as highly and then in by cell pectin the formation of bonds through et al., 1997). is completed, conducting xylem elements programmed cell death, and ordered in which and and are and 2000). factors and the cell to by the of by the are in the a that a the to with the of that all of the but not the secondary cell wall. The role of phytohormones in cambial cell division, primary cell wall expansion, and secondary wall formation has been reviewed by et al. and Mellerowicz et al. (2001). have the of an the developing vascular of pine and This to have a in cambial develop to their position the and cell the same to develop in a A Suc has been as well and may provide for xylem and phloem than have been to be involved in by with in a and or of the molecular that determine the differentiation of a cambial is the we can that these result in of gene which in turn the activity of transcription factors. In particular, considerable progress has been made in understanding the of transcription factors in The of genes have also the presence in the of that have been to be important in xylem gene expression et al., 2000). that can this and the to the genes xylem were to be involved in transcription during and 2000). Three-dimensional structure of the secondary cell wall of a The cell wall is different layer of cellulose which determine the mechanical and physical properties of the wood in that MFs may be (as in the primary cell or at a to the cell (as in layer and The ensures the between The layer is the of the only to and to of the total of the cell wall. This layer is as an between the primary cell wall and the and The with to the cell is to The layer is the layer in the secondary cell wall, and is the most with to mechanical The of the layer between and and for to of the total of the cell wall. The in this layer is to to the cell and can be even on mechanical section on The of the cellulose MFs in the layer can the physical and mechanical properties of the cell and even wood as a the with to the cell wood and the longitudinal of as in the of juvenile and wood The layer of the secondary cell wall, the is relatively only to The MFs are ordered in a but than in the and the is to with to the cell the newly wood cell to the deposition of lignin and cellulose in the secondary cell wall to the cell and it to longitudinally However, as the wood cell is to wood it thereby up a mechanical in the cell wall In wood this a the wood in the of a tree is in and However, as the wood layer a tangential on the wood present in the thereby the wood the tree and A, of a wood (Pinus showing the different of wood which can be present a tree of B, A higher view of the wood cells the between wood and wood cells have and cell that may the molecular an in which is needed for or a in water near the in bordered and even mechanical or as trees which have been to such a HW formation near the zone of mechanical et al., However, HW formation is also genetic as some species which not even even at a very Once genes in the have been by a molecular a of in cell death. little has been on the identification of the genes involved in this process. However, recent research has that in biosynthesis was in the are highly soluble and in the was to be highly with the of genes encoding the synthase and all of which are in the et al., the same time that these genes are in the in this et al. that in and from the to the with only present in the thereby that these and are for the by which HW future research should on the genes in the of different as well as the endogenous or molecular activity in this Wood among of the for and for is a of this This is to the of the cell that up the different and the structure of the and physical in wood characteristics a single tree are also a the in wood, to juvenile wood with from the to the particularly in the years of cambium and between and Wood can also be by from and by In the of cambial activity and is by et al., and In is in the growing and are for has cells and a from or fibers of large radial (Fig. is in the or cambial cell and expansion has from the small radial and large tangential wall in the wood cells, the is to xylem and so the of water The of one of wood cell to is between growing between and the following However, one growing this may be relatively or on the species. The from juvenile wood during the first years of a in trees and in the of and to mature wood is major in wood during a life (Fig. for wood to and as trees are that grow than their and are logged at an the of in the timber of the characteristics of with is a and a higher which to such wood and to wood is in to a orientation of the by or This of wood as of a developmental which to a or so as to the tree a more position (for review, see and In both and such is with radial growth of the and in is called as it in of the tree in on the of a is highly with more and cellulose than The of is up to 50% higher than that of In the of the cellulose fibers in the layer of the cell wall is is cell is and the In wood is called wood as it to in of the tree in the of a The lignin of is the cellulose is higher and is than that of The wood produced on the of a or to the wood may also be of a and can be as many properties between and wood The which wood formation is but may be a of the related to intrinsic growth direction and and particularly that of and et al., and A of wood in a is to be a major for major in wood (the in in an in longitudinal and with is more likely to during and fiber products of is also a for the wood industry as it radial, and tangential during the process. The most important by which wood a tree to to the during the cell maturation process. In the in the layer is higher to the cell than in to a of lignin between the a result of this in cell wall chemical the newly wood cells to expand However, as in a section for the cells are to cells, and in a of mechanical in a tree the wood therefore as these are In an layer between the and the called the or The layer is made up of cellulose, with an this layer in the longitudinal thereby a very strong of in the The result of wood cells is to the tree in the of and to the tree to a position in This considerable plasticity in wood as by the of these different of wood a single is to natural in the expression of This a unique opportunity to dissect the molecular and biochemical mechanisms such differences. Wood properties are known to among species and among species. This is and an opportunity to for wood superior product and is by chemical and and the to the trees are mature to wood of modern to the genes these should the time and with such by providing and to cell wall properties in a highly developmental process that is likely to a unique of genes, it is that the first to the molecular mechanisms of wood formation in is the secondary xylem of and is different in many both gymnosperm and angiosperm species should be to the process of wood formation. and are among the of their of their for genetic their small size and only a little than that of and the of genetic With to the conifer and the of and gene in conifer species as well as the homogeneous of the wood, it is likely that the in the few species will be of to research on other The formation of the secondary cell wall is driven by the coordinated expression of numerous genes specifically involved in the and deposition of lignins, and cell wall The of molecular in wood research has the identification and of a small of the molecular involved in this process (Higuchi, Savidge et al., 2000), such as involved in et al., and cellulose synthesis (Arioli et al., 2000), but also 2000), cell proteins et al., 2000), and 2000). This of is by the that from the genes for biosynthesis and only a have been the main structural are known to a certain virtually is known about their It is likely that some unknown of wood will from structural or regulatory genes that have not been and more at the gene and expression is needed in to the for wood and to which could be for leading to the of wood to genes that are related to wood formation are for tree species the of on the of putative gene by a of genes of known and that are during the formation of were providing a of genes for genetic of the wood A of the genes were also as et al., et al., We can that some of these unknown genes could be involved in wood formation. using is in with for the of and to a understanding of the molecular process of wood formation. In the expression of genes were during the stages in the differentiation process leading to mature xylem cells This also that many structural and regulatory genes of were a developmental are that underlie the anatomical, and chemical between or and et al., et al., et al., 2000), and The identification and of gene products in developing with a range of wood important genes chemical and of cell and cell therefore wood and in xylem of pine and et al., et al., 2000) also provide with essential of secondary cell wall formation. It is that one of the most highly genes in et al., and pine et al., were also at the in both species et al., et al., 2000). The presence of the of methyl and the complexity of gene for during The identification of genes specifically in the highly vascular cambium or xylem may also give with respect to the molecular processes involved in genes are thought to play in the genetic of wood genetic will precise of of these are to the identification of involved in wood formation and in the chemical and mechanical properties of these are involved in the genetic of wood needs to be by using in trees or or between and wood or in natural such is way in pine and for which for wood and properties have been on genetic It is that for the of wood formation, models are However, a understanding of the molecular mechanisms involved in cell wall biosynthesis and assembly can also from such as and to the of such models is the of of xylem formation in these plants to that in the tree. and more the view that the of the cellular, and developmental processes is the This also to secondary xylem formation. even wood properties can be highly for a it is to that the in wood properties are the result of natural in expression or biochemical properties of proteins, and are also of the cellular, and developmental by the of these have been for the and orientation of cellulose The formation of wood, although highly to also involves including and secondary thickening in the growth and can therefore be as a tree et al., This species is the most in with the With respect to wood formation, for (for review, see Fagard et al., and 2000) has structural and regulatory genes A gene a role in the of the orientation of microtubules in has been et al., et al., and is very likely to play a role in other species including tree species. alternative of in research in be to the of in tree by or identification of of wood development are also in the In cells can be to proteins and genes can be at different stages of xylem formation and et al., The of cambium and secondary xylem and the small size of these models it to large of for the molecular biology and of wood formation. In during the growth of of xylem may be by the providing highly material for molecular also the structure and complex of cambial wood and of of wood, trees will the main to the of the of a the understanding of the process by which the vascular cambium wood has very has been an wood and physical The understanding of the molecular and mechanisms of cambial activity and wood formation is as the main research which must including as well as the more biochemical and wood We and Chaffey for reading of the