Xylem Structure and Function
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1 Xylem Structure and Function Alexander A Myburg, North Carolina State University, Raleigh, North Carolina, USA Ronald R Sederoff, North Carolina State University, Raleigh, North Carolina, USA Vascular plants have evolved a highly specialized tissue, called xylem, which provides mechanical support and transports water, mineral nutrients and phytohormonal signals in the plant. Although it is the most abundant biological tissue on earth, much remains to be learned about the structure, function, development and evolution of xylem and of the genes that regulate the processes.. Introduction Introductory article Article Contents. Xylem Structure and Variability. Xylem Functions: Water Transport and Structural Support. Xylem Differentiation and Cell Wall Biosynthesis. Origin and Evolution of Xylem in Plants. Genetic Manipulation of Xylem Formation Introduction The earliest land plants were short, herbaceous plants that evolved from primitive, water-living ancestors. For these plants, the change from a predominantly aquatic to a terrestrial environment was accompanied by the need for additional structural support to keep the plants upright and the need for more efficient transport of water to the aboveground parts of the plants. Larger plant sizes also increased the need for co-ordination between remote plant parts. The development of specialized vascular tissues to fulfil these requirements played an important role in the evolution and adaptation of plants to the terrestrial environment. As the early land plants filled more and more terrestrial niches, the selective advantage of increased propagule dispersal associated with increase in height, and later competition for sunlight, increased the selection pressure for plants that could grow taller than other plants. The most successful plants were able to support more weight, transport water further and sustain growth for more than one season. The dramatic result of this evolutionary process is evident in the rapid increase of plants with secondary vascular tissues and arborescent growth form in a rather short evolutionary timespan ( million years ago). The stems and roots of modern plants are highly specialized conductive organs that can transport water, nutrients, photosynthetic products and chemical regulatory signals. These organs contain two types of conductive tissue: phloem and xylem. Phloem is the tissue that transports photosynthetic products and plant growth regulators (phytohormones) mainly from the leaves to the rest of the plant. Xylem is the tissue that transports water, mineral nutrients and phytohormones from the roots to the leaves and other plant organs. While herbaceous plants do contain xylem, it is a tissue that is most prominent in woody plants, especially trees. Most of our knowledge of xylem structure and function is based on woody plants. The most important functions of xylem include: (1) transport of water and mineral nutrients, (2) mechanical support and (3) storage of nutrients and water. Xylem Structure and Variability The cell types that make up xylem tissue show great variability across different plant groups, from species to species and even within the same plant. This section will focus on the structure and variability of xylem produced during primary and secondary growth in different plant groups. Xylem cell types The structural features of xylem are determined by the size, shape and distribution of xylem cell types and, in particular, by the shape and thickness of their cell walls. Cell wall structure affects cell type and characteristics Almost all plant cells produce primary cell walls. The major component of most primary walls in xylem is a disorganized network of cellulose fibrils, which allows the wall to stretch and expand as the cell grows. The secondary wall is deposited on the inner side of the primary wall during and after the cell has elongated or enlarged. The cellulose fibrils in the secondary wall are arranged in a regular fashion with alternating layers at fixed angles to the main axis of the cell (Figure 1). This reinforces the plant cell, while preserving the elastic nature of the primary wall. Most of the cell types in xylem can be distinguished based on the shape and features of the secondary cell wall. Xylem parenchyma cells store water, mineral nutrients and carbohydrates, and respond to wounding The cells responsible for most of the storage function of xylem are called parenchyma cells. Many xylem parenchyma cells have secondary lignified walls, particularly in 1
2 Xylem Structure and Function S3 (60 90 ) S2 (10 30 ) Secondary wall S1 (50 70 ) Primary wall Middle lamella Figure 1 Drawing of the secondary thickened wall of a mature tracheary element showing the orientation of cellulose microfibrils in the different layers of the wall. Note the designation of the secondary wall layers and the average microfibril angle of each layer: S1 is the outermost layer, S2 is the middle layer and S3 the innermost layer. Most of the wall thickness is determined by the thickness of the S2 layer (the relative thicknesses are: primary wall, 1%; S1,10 to 20%; S2, 40 to 90% and S3, 2 to 8%). Modified after Co te WA (1967) Wood Ultrastructure: An Atlas of Electron Micrographs. Seattle: University of Washington Press. wooden plants. In other cases, these cells have thin, primary walls with areas of plasmodesmata, called primary pit fields, through which cell-to-cell movement of water and mineral nutrients can take place. Mature xylem parenchyma cells in active xylem tissue retain a functional protoplasm and can store carbohydrates in the form of starch. These cells also play an important role in wound healing by forming callus and can differentiate to regenerate functional xylem cells. Sclerenchyma cells provide mechanical support, defence and water transport The cells involved in mechanical support and defence are specialized sclerenchyma cells. Fibres are long, narrow sclerenchyma cells, mostly with thick secondary walls (Figure 2b and c). They are mainly involved in the mechanical support function of xylem and defence against pathogens and herbivores. The conducting cells of xylem are called tracheary elements. There are two types of tracheary elements: tracheids (Figure 2a) and vessel elements (Figure 2d and e). Vessel elements are connected end-to-end through large perforations in their end walls to form a vessel. Tracheids are connected through large, circular bordered pits that are concentrated at the tapered ends (in the radial walls) of the cells (Figure 2a). Mature vessel elements and tracheids have no cellular contents and consist mainly of thickened secondary walls. 2 In most tracheary elements, almost the entire inner surface of the primary wall is covered by secondary wall, except for small areas called pits. In the lateral walls of such vessel elements, and the walls of tracheids (mostly radial walls), the pits occur in pit-pairs with the pits of neighbouring cells precisely aligned (Figure 3). A pit membrane, comprised of the primary walls of adjacent cells, separates the pits of each pit-pair. The inner aperture of the pit is often narrow and reinforced by extra secondary wall material to form a border. The outer aperture of each pit, which is bounded by the pit membrane, is usually wider to allow maximum conductance of water across the pit membrane. In most conifers, the central part of the pit membrane is thickened and lignified to form a torus (Figure 3). The torus is usually slightly larger than the aperture of the pit border and is impermeable to water. The outer part of the membrane (the margo) is digested to leave a porous network of cellulose fibrils through which water can move easily. Under certain circumstances, the torus can block one of the two inner apertures of the pit-pair and prevent the movement of water and air through the pit. In tracheids, this may serve to isolate cavitated tracheids and prevent the spread of embolisms. The end walls of vessel elements are modified into perforation plates (Figure 2d and e). Most vessel elements possess simple transverse perforation plates with only one large perforation, but compound perforation plates with two or more perforations occur. Simple perforations provide the least amount of resistance to water flow and, therefore, maximum conductance. Some primitive angiosperm families have slanted scalariform perforation plates. Primary growth Primary xylem occurs in separate vascular bundles Primary growth refers to the primary plant body that is formed through cell production by the apical meristems of the plant. In most but not all monocots (monocotyledons) and herbaceous dicots (dicotyledons), almost the entire plant body is the product of primary growth. In woody plants, this represents the innermost layers of xylem along the stem, branches and roots. The xylem tissue of young, unthickened stems and roots usually occurs in separate primary vascular bundles along with the phloem tissue. In dicots, the primary vascular bundles are typically arranged in a peripheral cylinder, while in monocots, the vascular bundles are scattered throughout the parenchymatous ground tissue of the plant body. The primary xylem in stems usually consists of early differentiating protoxylem, located on the inner side of the xylem, and late differentiating metaxylem on the outer side of the xylem. In most dicot and gymnosperm stems, a lateral meristem, called the vascular cambium, separates the primary xylem and phloem of each vascular bundle. This layer of cells develops as an extension of the procambium,
3 Bordered pits Simple pit Perforation plate Perforation (e) (d) (c) (b) (a) Figure 2 Drawing showing the relative sizes and shapes of some xylem cell types: (a) conifer tracheid with circular bordered pits, (b) fibre tracheid with bordered pits, (c) libriform fibre with simple pitting, (d) vessel element with scalariform perforations and (e) vessel element with a simple perforation. Note that conifer tracheids (3 to 5 mm) are usually much longer in relationship to fibres (0.8 to 2.3 mm) and vessel elements (0.2 to 1.3 mm). Secondary wall of adjacent cell Middle lamella Secondary wall Primary wall Border Inner aperture Torus Margo Figure 3 Structure of a bordered pit in the secondary wall of a conifer tracheid showing the modification of the pit membrane to a torus and margo. Note the loose network of cellulose fibrils that forms the margo and the secondary thickening of the central region to form the torus. In angiosperms, the pit membranes of bordered pits are usually not modified. strands of meristematic cells beginning just below the growth tip of the stem (and root). The vascular cambium will later give rise to secondary xylem and secondary phloem. Although some do have thickening meristems, the vascular cambium is absent in monocots. Secondary growth The secondary xylem of woody plants constitutes the major part of the stem, i.e. the wood. This section will focus on various aspects of wood structure that are directly related to the development and organization of secondary xylem. The development of secondary xylem Secondary xylem is formed by the vascular cambium All gymnosperms and woody dicots undergo secondary growth, which results in an increase in the diameter of the stem, branches and roots. The onset of secondary growth is characterized by the activation of cell division in the fascicular vascular cambium, i.e. the meristematic layer inside the vascular bundles. These cell divisions are 3
4 co-ordinated with cell divisions in the adjacent interfascicular region to produce a continuous cylinder of vascular cambium. Usually, secondary xylem is formed on the inner side and secondary phloem on the outer side of the cambium (Figure 4). Fusiform and ray initials give rise to the axial and radial components of xylem The vascular cambium consists of fusiform and ray initials. Fusiform initials divide longitudinally to give rise to the axial components of secondary growth, i.e. tracheary elements, fibres and axial parenchyma towards the inside and phloem cells towards the outside of the stem. Ray initials divide to form ray cells that run radially across the secondary vascular tissue. Rays serve to transport water, dissolved gases and organic nutrients radially in wood. As secondary growth proceeds, the cambial cylinder increases in diameter through lateral division of fusiform initials. Earlywood, latewood and growth rings The cambium of many woody plants exhibits periodic activity. In the spring and early summer (in temperate regions), conditions are conducive to active growth and relatively wide tracheary elements with thin walls are produced. Later in the summer and autumn, relatively narrow tracheary elements with thick walls are formed (Figure 4). These two types of xylem, called earlywood and latewood, are most commonly observed as concentric circles on the transverse section of the stem and are formed as a result of changes in the activity of the vascular cambium. When the activity of the vascular cambium is controlled by annual seasons (one ring is formed per year), these circles are true annual rings and the age of the stem can be deduced from the number of rings. In many regions of the world, particularly the tropics, growth rings do not always represent annual increments. More than one (or less than one) growth ring can be formed per year, for example when several dry and wet periods occur within a year. Heartwood and sapwood Wood cells have a limited lifetime in which they can actively transport water. After a variable number of years, cavitation occurs in most of the vessels and tracheids and the rest of the xylem cells in the growth ring die. These cells are then filled with resinous materials and polyphenols, and constitute the inner, often darker part of the woody stem called heartwood. The outer, water-conducting part of the stem is called sapwood. In many species, as sapwood is converted to heartwood, air-filled vessels in the sapwood are often sealed off by the intrusive growth of surrounding parenchyma cells. These intrusions are called tyloses and, together with the resinous materials, serve to prevent fungal growth in the empty vessel lumens. The outer, conducting part of the stem is called sapwood. Dicot versus conifer wood Woods are commonly classified as either hardwoods or softwoods. Hardwoods are angiosperm (dicotyledonous) trees, while softwoods are gymnosperm (conifer) trees. These two terms do not accurately express differences in the hardness or density of the wood, but are useful for the description of the basic structural differences between dicot and conifer wood. Ray Earlywood vessel Latewood vessel (a) Earlywood Latewood M M C M (b) Pith Primary xylem Secondary xylem Cambial zone Phloem Figure 4 Drawing of cross sections of young woody stems showing the cambial zone and secondary xylem development. (a) Dicot wood. (b) Conifer wood. Note the abrupt change in the size of tracheids from earlywood to latewood. M, differentiating xylem and phloem mother cells; C, cambial initial. 4
5 Dicot wood contains vessels, fibres, parenchyma and tracheids Dicot wood contains a greater number of cell types than conifer wood and the structure of dicot wood, therefore, varies more than that of conifer wood. The cell types of dicot wood include vessel elements, fibres and parenchyma cells. Tracheids are rare in dicots, but occur in some species such as oaks and chestnuts. The cell types in dicot wood are also more diversified in function; vessels and tracheids transport water, fibres provide structural support and parenchyma cells perform storage and regeneration functions. The feature that most distinguishes dicot wood from conifer wood is the presence of large-diameter vessel elements that disrupt the regular organization of the radial cell files derived from the cambial initials (Figure 4a). Two types of fibres are common in dicot wood: fibre tracheids and libriform fibres (Figure 2b and c). Fibre tracheids have thick walls with bordered pits. Libriform fibres have simple pits. Dicot wood generally contains larger rays than conifer wood and in most dicot species the rays consist only of ray parenchyma. Conifer wood consists mostly of regular files of tracheids Conifer wood is relatively simple in structure. The most distinctive features of conifer wood include: the regular organization of the radial files of tracheids, the absence of vessels and fibres and the small amount of wood parenchyma (Figure 4b). The long, tapered tracheids form the predominant cell type and fulfil both the mechanical and conductive functions of conifer wood. The majority of parenchyma cells in conifer wood are present in rays and, in some conifers such as the Pinaceae, in axial and radial resin ducts. Conifer rays consist primarily of ray parenchyma and, in some conifers, a smaller amount of ray tracheids. Resin ducts are large intercellular spaces surrounded by thin-walled parenchyma cells that excrete resin into the duct. The resin is believed to seal wounds and protect the plant against fungi and herbivores. Reaction wood Woody plants respond to bending induced by external forces, such as wind and gravity, by making reaction wood. Conifers produce reaction wood on the side of the branch or stem where the tissues are compressed (usually the underside) and it is therefore called compression wood. In dicots, reaction wood forms on the side under tension (usually the upper side) and it is called tension wood. Compression wood has thicker cell walls, higher lignin content and is darker than normal conifer wood. Tension wood is characterized by the presence of gelatinous fibres, low lignin content and high cellulose content. The purpose of reaction wood is to reorient bent stems and branches to allow optimal light exposure of the tree canopy. Secondary thickening in monocots The majority of monocots are herbaceous, which means that the primary xylem has to fulfil all the requirements of water transport that the plant may encounter throughout its lifetime. However, some monocots do undergo thickening of the primary stem. In bamboos and other monocot species with wide stems, a broad region of mitotic activity, called the primary thickening meristem, is responsible for radial and tangential expansion of the primary stem. Very few examples exist of truly woody monocots. In woody monocot genera such as Yucca and Dracaena, the activity of a secondary thickening meristem in the outer cortex of the stem is responsible for anomalous secondary growth. Arborescent monocots such as palms undergo diffuse secondary growth through the division of cells in the ground parenchyma of the stem. Xylem Functions: Water Transport and Structural Support Water transport A gradient of water potential drives water transport Despite a large amount of research on this topic, the precise mechanism of water transport in plants is still debated. The experimental evidence strongly suggests that water transport in plants is driven by a gradient of water potential that exists between the air surrounding the leaves at one end and the water that surrounds the roots at the other. These two extremes are connected by the xylem, which supports a water column that extends from the roots to the leaves. Air usually has a very negative water potential (even when the humidity is very high). As the leaves of the plant lose water to the air, the water potential becomes more negative inside leaf cells. This causes water to gradually move from xylem cells to leaf cells. The water molecules inside the water columns of the capillary xylem elements are pulled upwards by cohesion forces when water molecules at the top of the columns move out into the aerial parts of the plants. This is known as the cohesion tension theory of sap ascent. Adhesion, cohesion and tension forces act on the water column The upward movement of the water column is counteracted by three forces: (1) the weight of the water column, (2) adhesion of water to the cell walls of tracheary elements and (3) adhesion of the water to soil particles. The upward movement of the water molecules in each tracheary element will cause tension in the water column, causing it to become narrower. During times of high transpiration, the negative pressure inside tracheary elements can become strong enough to cause these cells to collapse inward. 5
6 Vessel elements and tracheids possess secondary thickened walls that serve to reinforce the walls and prevent inward collapse under the tremendous forces produced inside the tracheary element. Water columns can break The ability of tracheary elements to allow movement of water is called conductance. The conductance of a tracheary element is related to the fourth power of the radius of the element (known as the Hagen Poiseuille Law). This means that a slight increase in diameter of the element will significantly increase the conductance. Indeed, this seems to have been a major driving force in the evolution of tracheary elements. However, under certain circumstances it is beneficial to possess tracheary elements with small diameters. In such elements, hydrogen bonding of water molecules to the wall (adhesion force) serves to reinforce and strengthen the water column. If the tension in the water column becomes sufficiently strong, however, the water column can break (cavitate) and an embolism ( air bubble ) will form in the element. This problem is more serious in large-diameter elements than small-diameter elements. In tracheids, the embolism can expand to fill the whole cell, but the surface tension of water will prevent it from passing through the pit membrane. In vessels, embolisms can spread from element to element through the perforations that link consecutive vessel elements. The whole vessel will then become dysfunctional for water transport. Tracheids and vessel elements are adapted for optimal conductance Tracheids are generally much longer than vessel elements. This reduces the number of pit membranes that a water molecule has to cross on its way to the leaves. Tracheids also have long-tapered ends to allow the maximum number of pit-pairs between consecutive cells. Vessel elements are much shorter than tracheids, but they are connected endto-end to form long vessels. Gymnosperm tracheids tend to be wider than those of angiosperms, where most of the water transport occurs through large-diameter vessel elements. Angiosperms combine the structural and water-conducting benefits of small-diameter and largediameter tracheary elements. Most of the water volume is transported by large-diameter vessels when water is readily available, while small-diameter vessels and tracheids (in some dicots) are used when the water column is under great tension and greater protection against cavitation is required. Structural support The aerial parts of all terrestrial plants require mechanical support. This is provided in large part by xylem tissue in the stem and branches. The mechanical support function of xylem is most prominent in the stems of trees, which include some of the largest living organisms on earth. Cell walls form the basic unit of structural support The basic unit of structural support in plants is the mechanical support provided by the cell wall of each cell in the plant body. Cell walls consist mostly of cellulose microfibrils. Cellulose fibrils can be very strong; stronger than steel, silk or nylon. This makes cell walls strong enough to resist internal forces (turgor) as well as externally applied forces (tension). Additional rigidity and compressive strength is provided by lignin, especially in tissues (such as xylem) that accumulate lignin. Xylem contains several cell types with structural support functions Fibres provide most of the mechanical support in dicot xylem. The structure of the fibre walls allows this cell type to support weights of up to kg mm 2 2. More importantly, fibres are elastic enough to retain their original length after subjection to tension forces of this magnitude. Vessels and tracheids also contain secondary thickened walls and therefore contribute to structural support in xylem. In conifer wood, all the structural support is provided by tracheids. Wood is a complex material The woody stems of large trees provide the most spectacular examples of structural support in plants. Wood in living tree stems is structurally complex, with several levels of organization. At the molecular level, wood is comprised of crystalline cellulose embedded in a matrix of hemicellulose and lignin, a highly crosslinked phenolic polymer. The cellulose fibrils in the secondary wall are deposited in layers, each layer with a different preferred microfibril angle (Figure 1). At the cellular level, the xylem cells in wood are arranged in cylinders parallel to the long axis of the stem. Finally, above the cellular level, the growth rings form concentric layers of wood tissue with different wall and lumen dimensions. This makes wood a layered structural composite, which is much more complex than reinforced concrete. Xylem Differentiation and Cell Wall Biosynthesis The developmental process in which procambial and cambial initials differentiate into mature xylem cells is called xylogenesis. This process can be as short as four days 6
7 in primary xylem and from days in secondary xylem. Xylogenesis typically includes the following phases: (1) cell division and enlargement, (2) cell wall thickening, (3) lignification and (4) programmed cell death. Cell wall biosynthesis is an integral part of xylem formation. The basic chemical components and organization of xylem cell walls are known, but little is known of the mechanisms by which they are synthesized and organized to form the highly complex cell wall. This section will outline the phases of xylem differentiation and the formation of xylem cell walls, which form the major part of mature xylem cells. Xylem cells are derived from apical and lateral meristems Tracheary elements are derived from either the procambium (primary xylem) or vascular cambium (secondary xylem). The differentiation of cambial initials into xylem elements is thought to be initiated by plant hormones. The immature xylem cells have dense protoplasm, small vacuoles and thin primary walls (Figure 4). Soon after cell division, these cells undergo cell elongation and an increase in the size of the vacuole and nuclei. Most xylem cell walls undergo secondary thickening The deposition of secondary walls begins sometime before tracheary elements and fibres reach their full size. The cellulose, lignin, hemicellulose and protein components of the secondary wall are synthesized and deposited cooperatively during secondary wall thickening. The onset of secondary wall thickening is associated with the formation of arrays of microtubules under those regions of the plasma membrane where active secondary wall deposition will take place. Microtubules may play a role in defining the pattern of secondary walls by guiding dictyosome-derived vesicles with cell wall material to the sites of deposition on the cell membrane. Cellulose microfibrils are produced at the membrane surface of the cell by complex rosette structures, which consist of several different proteins. The movement of these rosette complexes in the plasma membrane may also be directed by microtubules. The cell walls and intercellular regions of xylem cells are lignified Following secondary thickening of the xylem cell walls, lignin is deposited between the newly formed tracheary elements and within their walls. The area between the cells, called the middle lamella, and the primary walls are rapidly lignified, followed by a more gradual lignification of the secondary walls. Lignin is a very complex, crosslinked, three-dimensional polymer of aromatic phenolic monomers, called cinnamyl alcohols. The lignin monomers are delivered to the cell wall via Golgi and endoplasmic reticulum-derived vesicles and polymerized into lignin by wall-bound enzymes. The aromatic nature of the lignin monomers makes lignin hydrophobic. Lignin, therefore, provides a hydrophobic inner surface to the cell wall that facilitates water transport. The three-dimensional nature of the lignin polymer provides rigidity and compressive strength to the cell wall, while the chemical stability of lignin provides protection against pathogens. Tracheary elements undergo programmed cell death At the completion of secondary wall deposition and lignification, tracheary elements undergo autolysis, an example of programmed cell death in higher plants. Soon after the initiation of secondary thickening, hydrolytic enzymes (DNAases, RNAases and proteases) start accumulating in the vacuole. The autolytic process is initiated when the tonoplast ruptures, causing the hydrolytic enzymes to spill out into the cytoplasm. This leads to the complete degradation of the cell contents and partial digestion of the unprotected regions of the primary wall. Only regions covered by lignified secondary wall material are protected from degradation. The end walls of differentiating vessel elements are degraded at the perforation sites to allow direct cell-to-cell movement of water and nutrients. Only regions covered by lignified secondary wall material are protected from degradation. Pit membranes are often partially degraded to leave mats of cellulose fibrils (Figure 3). This enhances the movement of water through pit-pairs, which is the only way water can enter and leave tracheids. Origin and Evolution of Xylem in Plants Vascular plants (Tracheophyta) are characterized by the presence of xylem tissue with lignified cell walls. Modern vascular plants are ferns, gymnosperms and angiosperms. Mosses, liverworts and hornworts (Bryophyta) do not contain xylem. Tracheid-like cells, called hydroids, are present in certain bryophytes, but lignified cell wall thickenings are absent in these plants. This section will outline the major trends of xylem evolution in vascular plants. Evolution of primary xylem Tracheids were present in the first vascular land plants It is widely accepted that the first land plants evolved from green algae (Chlorophyta) and that these plants were adapted to aquatic or semiaquatic environments. The evolution of conducting tissue was closely associated with 7
8 the adaptation of plants to fully terrestrial environments. The acquisition of xylem tissue allowed plants to supply water and mineral nutrients to those parts of the plant body exposed to the desiccating environment of the air. One of the earliest known fossilized land plants, Cooksonia (present as early as 420 million years ago in the Mid- Silurian Period), had tracheids with annular secondary thickenings. Vessel elements and fibre tracheids evolved from tracheids Vessel elements evolved independently from tracheids in several groups of flowering plants, i.e. the conversion of tracheid end walls to perforation plates had a polypheletic origin. Fossil evidence of the early evolving vessel elements is very scarce. It is assumed that vessel elements evolved from tracheids with scalariformly reinforced walls and that these cells gave rise to the short vessel elements with transverse, simple perforation plates and wide lumens. Fibres also evolved independently in many angiosperm families. Fibre tracheids evolved very early in angiosperm history, while libriform fibres with simple pits appeared later. Evolution of secondary xylem Woody plants appeared early in the history of land plants The ability to produce secondary vascular tissues evolved soon after the appearance of the first vascular land plants. Bifacial cambium was present in the Progymnospermopsida in the Devonian Period (approximately 370 million years ago). It is still highly debatable whether the first angiosperms that evolved from the progymnosperms were woody or herbaceous plants. It appears however that most present day herbaceous angiosperms are able to form secondary tissues, although most usually flower and die early, precluding much secondary growth. Secondary xylem increased the lifespan of plants The ability to produce secondary xylem had profound consequences for early vascular plants. It greatly increased the lifespan of plants by allowing plants to essentially form a new water-conducting system each year that replaced the non-functional xylem elements from previous years. The increase in lifespan enabled the existence of taller plants and increased the need for long-distance conductance and mechanical support. The major trends of xylem evolution (the shift towards vessel elements, simple perforations and libriform fibres) are thought to be associated with the increased efficiency of water transport in xylem and, to a lesser degree, the increased demand for mechanical support in plants. Genetic Manipulation of Xylem Formation The content and composition of xylem cell walls affect the commercial value of many biological materials, such as wood and plant fibres, as well as many food crops, such as fodder, cereals, fruits and vegetables. The potential to improve the properties of these plants has motivated studies dedicated to the modification of xylem cell walls. Xylem properties are specified by a large number of genes and proteins The properties of wood and the xylem in herbaceous plants result from the content, composition and location of xylem cells and their walls. Except for the wall, tracheary elements retain little or no material of the living cells from which they are derived. The composition and structure of xylem cell walls are determined by the coordinated expression of a large number of genes and proteins during xylogenesis. Variation in the developmental programme and levels of expression of individual genes determine the variation in cell wall architecture within and between different species. Therefore, knowledge of the genes involved in this process and the mechanisms by which they are controlled could lead to the ability to manipulate the properties of xylem. Although the general composition and structure of xylem cell walls is known, very little is known of the organization and biosynthesis of cell wall components. Xylem cell walls contain hundreds of proteins and enzymes involved in the formation of the primary cell wall, which provide the framework for the synthesis of the secondary wall. Biosynthesis of the secondary wall involves precisely regulated formation of cellulose microfibrils, assembly of hemicellulose cellulose complexes and polymerization of a network of the phenolic polymer lignin. Work is progressing rapidly to identify important genes and proteins in these processes, but only a few genes have been studied sufficiently to establish their specific roles. New technologies allow rapid progress in the genetic manipulation of xylem Studies of model plant systems, such as Arabidopsis, Zinnia, tobacco and maize have been important in identifying specific genes and proteins involved in cell wall formation. Genetic and biochemical studies of cotton and forest trees have identified some important genes for the formation of cellulose and lignin. Most recently, many laboratories have decided to use high-throughput automated techniques to identify all of the expressed genes of higher plants and to learn their function. This approach, called genomics, is expected to rapidly advance the knowledge of the genes and proteins forming the primary 8
9 and secondary cell walls of xylem. With this knowledge, the modification of xylem in commercially important plants will become a process of rational design. Further Reading Boudet AM, Lapierre C and Grima-Pettenati J (1995) Tansley Review no 80: Biochemistry and molecular biology of lignification. New Phytologist 129: Carlquist JS (1975) Ecological Strategies of Xylem Evolution. Berkeley, CA: University of California Press. Delmer DP and Amor Y (1995) Cellulose biosynthesis. Plant Cell 7: Fahn A (1990) Plant Anatomy, 4th ed. New York: Pergamon Press. Fukuda H (1996) Xylogenesis: initiation, progression and cell death. Annual Review of Plant Physiology and Molecular Biology 47: Higuchi T (1997) Biochemistry and Molecular Biology of Wood. Berlin: Springer-Verlag. Ingrouille M (1992) Diversity and Evolution of Land Plants. London: Chapman & Hall. Mauseth JD (1988) Plant Anatomy. Menlo Park, CA: Benjamin/ Cummings. Whetten RW, MacKay JJ and Sederoff RR (1998) Recent advances in understanding lignin biosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 49: Zimmermann MH (1983) Xylem Structure and the Ascent of Sap. Berlin: Springer-Verlag. 9
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