Annu. Rev. Plant Biol. 2002. 53:183202 DOI: 10.1146/annurev.arplant.53.100301.135245 Copyright c 2002 by Annual Reviews.

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VASCULAR TISSUE DIFFERENTIATION AND PATTERN FORMATION IN PLANTS

Annu. Rev. Plant Biol. 2002.53:183-202. Downloaded from arjournals.annualreviews.org by Michigan Technological University - J. R. VAN PELT LIBRARY on 11/11/07. For personal use only.

Zheng-Hua Ye
Department of Botany, University of Georgia, Athens, Georgia 30602; e-mail: zhye@dogwood.botany.uga.edu

Key Words auxin, procambium, positional information, venation, xylem s Abstract Vascular tissues, xylem and phloem, are differentiated from meristematic cells, procambium, and vascular cambium. Auxin and cytokinin have been considered essential for vascular tissue differentiation; this is supported by recent molecular and genetic analyses. Xylogenesis has long been used as a model for study of cell differentiation, and many genes involved in late stages of tracheary element formation have been characterized. A number of mutants affecting vascular differentiation and pattern formation have been isolated in Arabidopsis. Studies of some of these mutants have suggested that vascular tissue organization within the bundles and vascular pattern formation at the organ level are regulated by positional information.

CONTENTS
INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VASCULAR TISSUES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VASCULAR PATTERNS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Vascular Tissue Organization Within a Vascular Bundle . . . . . . . . . . . . . . . . . . . . . Vascular Tissue Organization at the Organ Level . . . . . . . . . . . . . . . . . . . . . . . . . . . MODEL SYSTEMS FOR STUDYING VASCULAR DEVELOPMENT . . . . . . . . . . Coleus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Zinnia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Arabidopsis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . APPROACHES USED FOR STUDYING VASCULAR DEVELOPMENT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VISUALIZATION OF VASCULAR TISSUES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . PROCESSES OF VASCULAR DIFFERENTIATION . . . . . . . . . . . . . . . . . . . . . . . . . Formation of Procambium and Vascular Cambium . . . . . . . . . . . . . . . . . . . . . . . . . Initiation of Xylem Differentiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cell Elongation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Secondary Wall Thickening . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cell Death . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VASCULAR PATTERN FORMATION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Vascular Bundles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1040-2519/02/0601-0183$14.00 184 184 185 185 185 186 186 186 187 187 188 188 188 190 192 192 193 193 193

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YE Vascular Patterning at the Organ Level . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 195 CONCLUSIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197

INTRODUCTION
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Plant vascular tissues, xylem and phloem, evolved as early as the Silurian period some 430 million years ago. Evolution of vascular tissues solved the problem of long-distance transport of water and food, thus enabling early vascular plants to gradually colonize the land (71). In primitive vascular plants, vascular tissues are organized in a simple pattern such that xylem is located at the center and phloem surrounds xylem. With the evolution of diverse vascular plants, vascular tissues also evolved to have a variety of organizations (28). In a given cross section of primary stems and roots, the most prominent variation of anatomical structures among different species is the organization of vascular tissues. In the stems of woody plants, the vascular tissue, secondary xylem or wood, provides both mechanical strength and long-distance transport of water and nutrients, which enables shoots of some woody plants to grow up to 100 m tall. Vascular tissues have long been chosen as a model for study of cell differentiation (48, 73, 79). In this review, I rst briey describe the general anatomical features of vascular tissues that will be useful to readers who are not familiar with this subject, and then devote my discussion mainly to the latest progress and current status of the study of vascular differentiation and pattern formation. For additional information, readers are referred to several recent excellent reviews that cover additional aspects of vascular differentiation and pattern formation (9, 1113, 23, 34, 35, 64, 74, 78).

VASCULAR TISSUES
Vascular tissues are composed of two basic units, xylem and phloem. Xylem transports and stores water and nutrients, transports plant hormones such as abscisic acid and cytokinin, and provides mechanical support to the plant body. Phloem provides paths for distribution of the photosynthetic product sucrose and for translocation of proteins and mRNAs involved in plant growth and development. Xylem is composed of conducting tracheary elements and nonconducting elements such as xylary parenchyma cells and xylary bers. Tracheary elements in angiosperms typically are vessel elements that are perforated at both ends to form continuous hollow columns called vessels (Figure 1a). Tracheary elements in gymnosperms are tracheids that are connected through bordered pits to form continuous columns. Phloem is composed of conducting sieve elements and nonconducting cells such as parenchyma cells and bers. Sieve elements of nonowering plants are sieve cells that are connected with each other through sieve areas. Sieve elements of most owering plants are sieve tube members that are connected through sieve plates to form continuous columns (28, 58).

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Vascular tissues can be formed from two different meristematic tissues, procambium and vascular cambium. During the primary growth of stems and roots, procambial initials derived from apical meristems produce primary xylem and primary phloem. Vascular cambium initials, which are originated from procambium and other parenchyma cells when plants undergo secondary growth, give rise to secondary xylem, commonly called wood, and secondary phloem. Vascular cambium is typically composed of two types of initials: fusiform initials that produce tracheary elements and xylary bers in the longitudinal system of wood and ray initials that produce ray parenchyma cells in the transverse system of wood (28, 58).

VASCULAR PATTERNS Vascular Tissue Organization Within a Vascular Bundle

There is great plasticity in the organization of vascular tissues within a vascular bundle as long as vascular tissues are functional for transport. The common vascular organization within a bundle is a parallel placement of xylem and phloem, a pattern called collateral vascular bundles (Figure 1c). In some families such as Cucurbitaceae and Solanaceae, xylem is placed in parallel with external phloem and internal phloem, a pattern called bicollateral vascular bundles. Several lesscommon vascular tissue organizations were also evolved in vascular plants. In some monocot plants such as Acorus and Dracaena, phloem is surrounded by a continuous ring of xylem, a pattern called amphivasal vascular bundles (Figure 1d ). In contrast, amphicribral vascular bundles, which are found in some angiosperms and ferns, have xylem surrounded by a ring of phloem (58).

Vascular Tissue Organization at the Organ Level

Conducting elements of xylem and phloem form continuous columns, a vascular system throughout the plant body for transport of water, nutrients, and food. Similar to the diverse organizations of vascular tissues seen within vascular bundles, vascular plants have also evolved a diversity of patterns for placement of vascular bundles in the stele. In primary stems and roots, two major patterns for placement of vascular bundles are recognized. One is the protostele in which xylem forms a solid mass at the center of the stele and phloem surrounds xylem. This is considered to be a primitive type of vascular pattern that is commonly seen in shoots of many nonseed vascular plants and in the primary roots of many dicot plants. The other is the siphonostele in which individual vascular bundles are arranged in the stele. Based on the arrangement of vascular bundles in the stele, siphonostele is generally grouped into two major patterns. In one, vascular bundles are organized as a ring in the stele, a pattern called eustele, which is mainly seen in stems of dicots and in roots of monocots. In the other, vascular bundles are scattered throughout the ground tissue, a pattern called atactostele, which is commonly seen in stems

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of monocot plants. Siphonostele may have evolved from the protostele by gradual replacement of the solid mass of xylem at the center with parenchyma cells (58). In leaves, vascular bundles, commonly called veins, are organized in distinct patterns among different species. Leaves of most dicot plants have a midvein and a network of minor veins. Leaves of most monocot plants typically have veins run in parallel. Ginkgo leaves have an open dichotomous venation pattern. Many subtle variations of leaf venation patterns among different species have been recorded (76).

MODEL SYSTEMS FOR STUDYING VASCULAR DEVELOPMENT Coleus

It is apparent that the complexity of vascular tissues and their organizations presents a big challenge for studying the molecular mechanisms underlying vascular differentiation and pattern formation. At the same time, vascular tissues represent a model for understanding many aspects of fundamental biological questions regarding cell specication, cell elongation, cell wall biosynthesis, and pattern formation. To study the different aspects of vascular development, it is ideal to choose simple or genetically manipulable systems. One of the early systems used for vascular study is Coleus in which the stems were used to study roles of auxin and cytokinin in the induction of xylem and phloem formation (3, 4). The advantage of Coleus is that the stems are big enough for easy excision of vascular tissues and subsequent analysis of effects of external factors on vascular differentiation. However, this system has been limited to physiological studies.

Zinnia
Tissue culture has long been used to study the effects of hormones on xylem and phloem differentiation (3). The most remarkable in vitro system developed so far is the zinnia in vitro tracheary element induction system (34). In this system, isolated mesophyll cells from young zinnia leaves can be induced to transdifferentiate into tracheary elements in the presence of auxin and cytokinin (Figure 1b). The advantage of this system is that isolated mesophyll cells are nearly homogeneous, and the induction rate of tracheary elements can reach up to 60%. Thus the biochemical and molecular changes associated with the differentiation of a single cell type, tracheary elements, can be monitored. A number of genes associated with tracheary element formation have been isolated and characterized by using this system (34, 61). The zinnia in vitro tracheary element induction system presents an excellent source for isolation of genes essential for different aspects of tracheary element differentiation, including cell specication, patterned secondary wall thickening, and programmed cell death.

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Arabidopsis
With the introduction of the model plant Arabidopsis as a genetic system for studying plant growth and development, Arabidopsis has been adopted as a powerful system for genetic dissection of vascular differentiation and pattern formation. Unlike the zinnia system, which is limited to the study of one cell-type differentiation, Arabidopsis can be used to study not only the differentiation of multiple cell types in the vascular tissues but also vascular differentiation and pattern formation at the organ level. Recent studies of Arabidopsis mutants have opened new avenues for understanding the molecular mechanisms regulating various aspects of vascular development, such as alignment of vascular strands (17, 69), formation of a network of veins in leaves (16, 18, 19, 24, 43, 52, 69), division of procambial cells (55, 81), differentiation of primary and secondary xylem (36, 105), and organization of vascular tissues within the bundles in leaves (59, 60, 95, 96, 104) and stems (104). It is apparent that the Arabidopsis system is still not fully exploited, and novel mutant-screening approaches should be employed to isolate more mutants affecting various aspects of vascular differentiation and pattern formation.

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APPROACHES USED FOR STUDYING VASCULAR DEVELOPMENT

Vascular development has traditionally been studied using physiological, biochemical, and molecular approaches. Early physiological studies have established that the plant hormones auxin and cytokinin are important for vascular differentiation (3, 77). A number of proteins and genes involved in different stages of tracheary element formation such as secondary wall thickening and cell death have been characterized using biochemical and subtractive hybridization approaches (34). With the recent advance of molecular tools and the introduction of the Arabidopsis genetic system, many new approaches have been applied to the research of vascular differentiation. One powerful approach that goes beyond Arabidopsis is the large-scale sequencing of the expressed sequences from cambium and secondary xylem of pine (2) and poplar (86). Categorization of the genes expressed in the vascular cambium and secondary xylem by microarray technology (42a) will provide invaluable tools for further study of proteins involved in the differentiation of different cell types in wood. A similar approach using PCR-amplied fragment length polymorphisms has been applied to the zinnia system for isolation of genes involved in the differentiation of tracheary elements (61). Another powerful approach is to isolate mutants with defects in vascular development. Isolation of genes that regulate vascular differentiation and pattern formation is essential for the study of vascular development because these genes can be used as tools for isolation of upstream and downstream genes by molecular and genomic approaches such as direct target screening, microarray, and yeast twohybrid analysis. Many Arabidopsis mutants affect vascular patterning or normal formation of vascular strands (Tables 14), but none completely block the vascular

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cell differentiation, presumably because of the potential lethality to plants. New mutant-screening approaches such as temperature-sensitive mutants and T-DNA enhancer trap lines should be exploited.

VISUALIZATION OF VASCULAR TISSUES

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The most prominent feature of vascular tissues is the presence of tracheary elements with thickened secondary wall and lignin deposition. Tracheary elements can be easily visualized by histological staining with dyes such as toluidine blue and phloroglucinol-HCl (66). For large organs such as stems of Arabidopsis, free-hand sections stained with the dyes often give satisfactory anatomical images (92). For high resolution, thin or ultrathin sections should be sought (66). For observation of leaf venation pattern, leaves can be cleared with chloral hydrate and then observed under light microscope (16, 57). Recently, confocal microscopy, which can give high-quality images, has been applied to visualize vascular tissues in leaves and roots. After staining with basic Fuchsin, the lignied tracheary elements in leaves and roots can be readily seen under a confocal microscope (17, 25). Molecular markers can be used to visualize the differentiation of vascular tissues. For example, the promoters of ATHB8 (6) and phosphoinositol kinase (27) genes, which are expressed in procambial cells, can be used as early markers of vascular differentiation. The promoter of TED3 gene, which is specically expressed in xylem cells (44), can be used as a marker of xylogenesis.

PROCESSES OF VASCULAR DIFFERENTIATION

Owing to the existence of multiple cell types and various organizations of vascular tissues, one can imagine that the molecular mechanisms controlling the vascular differentiation are also complicated, and many genes may be involved in vascular development. Because most of the research on vascular differentiation has been focused on xylem differentiation and very few studies have been done on phloem differentiation (90), I focus my discussion on the processes of xylem formation as follows: formation of procambium and vascular cambium, initiation of xylem differentiation, cell elongation, secondary wall thickening, and cell death.

Formation of Procambium and Vascular Cambium

Vascular tissues are differentiated from meristematic cells: procambial cells during primary growth and vascular cambium cells during secondary growth. Procambial cells in roots and stems are derived from apical meristems. Procambial cells in leaves are formed during very early stages of leaf development. It is clear that the sites for procambial cell initiation determine the pattern of vascular organization and that the activity of procambial cells controls the differentiation of vascular tissues. The central question is how molecular signals mediate the initiation of

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procambial cells and promote their division, which continuously provides precursor cells for differentiation of xylem and phloem. It has long been proposed that auxin, which is polarly transported from shoot apical meristem and young leaves, induces formation of procambial cells. Early physiological studies have clearly demonstrated that the signals for induction of procambial cell formation are derived from apex and that exogenous auxin could replace the function of apex in the induction of procambial cell formation (3, 77). Roles of auxin in the induction of procambial cell formation have been supported by genetic studies in Arabidopsis mutants. Mutation of the MP gene, which encodes an auxin-response factor, disrupts the normal formation of continuous vascular strands (10, 41, 69). Mutants such as pin1 (36, 67) and gnom (52, 85) with defects in auxin polar transport show dramatic alterations in vascular differentiation. The PIN1 gene encodes an auxin efux carrier (36), and the GNOM gene encodes a membraneassociated guanine-nucleotide exchange factor for an ADP-ribosylation factor G protein that is required for the coordinated polar location of PIN1 protein (85). Further studies on the roles of additional auxin polar transport carriers and auxin response factors will help us understand the roles of auxin in procambial cell formation. Cytokinin is essential for promoting the division of procambial cells (3). Mutation of the WOL/CRE1 gene, which encodes a cytokinin receptor (47, 55), leads to differentiation of all procambial cells into protoxylem (55, 81). Crossing of wol with fass, a mutant with supernumerary cell layers, shows that WOL is not essential for phloem and metaxylem formation, indicating that WOL is involved in promotion of procambial cell division. WOL is localized in procambial cells in roots and embryos (55). Because there are several other WOL-like cytokinin receptors in the Arabidopsis genome (82), it will be interesting to investigate whether they are also involved in promoting procambial cell division. Little is known at the molecular level about how auxin and cytokinin induce procambial cell formation. Because procambial cells are dividing cells, auxin and cytokinin are likely to stimulate cell proliferation by regulating the cell cycle progression (22a,b). Recently, investigators have shown that an inositol phospholipid kinase, which is involved in the synthesis of phosphoinositide signaling molecules, is predominantly expressed in procambial cells (27). Because auxin induces the formation of phosphoinositides that may be involved in cell proliferation (29), phosphoinositides might be involved in the auxin and cytokinin signal transduction pathways, leading to procambial cell formation. The auxin response factors such as MP are obvious candidates for involvement in auxin signaling, and further characterization of their functions will be essential for understanding how auxin initiates procambial cell formation. A number of other genes such as ATHB8 (6) and Oshox1 (80) are expressed in procambial cells, but their precise roles in procambial cell formation are not known. Overexpression of ATHB8 leads to overproduction of vascular tissues, suggesting that ATHB8 might be involved in stimulation of procambial cell activity (7). Vascular cambium, a lateral meristem, is derived from procambial cells and other parenchyma cells, such as interfascicular cells in stems and pericycle cells

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in roots, when organs initiate secondary growth. Auxin may regulate cambium activity (3). Recently, auxin has been shown to be distributed in a gradient across the cambial zone of pine stems (93, 94). In addition, reduction in auxin polar transport in the inorescence stems of the i1 mutants leads to a block of vascular cambium activity at the basal parts of stems (103, 105). The block of vascular cambium activity in the i1 mutants is associated with reduced expression of auxin efux carriers PIN3 and PIN4 (106), suggesting important roles of polar auxin ow in vascular cambium activity. Because many auxin efux carrier homologues have been identied in the Arabidopsis genome, it will be important to investigate which carriers play central roles in the formation of vascular cambial cells. Induction of vascular cambial cell formation by auxin is likely mediated through the protein kinase PINOID (21) because mutation of the PINOID gene completely abolishes the vascular cambium formation (R. Zhong & Z-H. Ye, unpublished observations). Cytokinin is considered essential for the continuous division of vascular cambium cells, which supply precursor cells for differentiation into xylem and phloem (3). Because Arabidopsis stems and roots undergo secondary growth (7, 26, 102), it will be interesting to investigate whether WOL or other cytokinin receptor homologs are involved in the regulation of vascular cambium cell division in Arabidopsis. Dissection of the signaling transduction pathways of auxin and cytokinin that lead to vascular cambium formation is essential for our understanding of vascular cambium development.

Initiation of Xylem Differentiation

Procambium and vascular cambium are polar in terms of the nal fates of their daughter cells. The daughter cells may become either xylem precursor cells or phloem precursor cells, depending on their positions. This suggests that the cambial cells at different positions receive different signals that specify different cell fates. Auxin may act as a patterning agent for differentiation of vascular tissues. Auxin is distributed in a gradient across the cambial region (93, 94), indicating that different levels of auxin together with other signaling molecules such as cytokinin are important for vascular cell differentiation (3, 4, 77, 78). Transgenic studies have shown that alterations of endogenous auxin level dramatically affect xylem formation (50, 75). Although the phenotype of the wol mutant suggests that cytokinin is not directly involved in xylem differentiation, in vitro studies in zinnia indicate that both auxin and cytokinin are required for induction of xylem cell formation. It is possible that other WOL-like genes play roles in xylem cell differentiation. In addition to auxin and cytokinin, other factors such as brassinosteroid (49, 98, 99) and phytosulfokine, a peptide growth factor (56), might play important roles in the stimulation of xylogenesis. Little is known about the signal transduction pathways of auxin and cytokinin, which lead to xylem cell formation. MP, an auxin response factor, is likely involved in this process because mutation of the MP gene results in misaligned xylem strands (41, 69). Many other auxin response factors have been identied (39), and studies of their functions will likely help us to further understand vascular cell differentiation. Several other transcription factors such as Arabidopsis ATHB8

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(6, 7), rice Oshox1 (80), and aspen PttHB1 (42) might also play roles in xylem cell differentiation. Auxin-insensitive mutants axr6 (43) and bodenlos (40) are defective in venation pattern, and their corresponding genes are likely involved in auxin signaling pathways important for vascular differentiation. In addition, the maize wilted mutant causes a partial block of metaxylem cell formation (68) (Figures 2a,b), and the Arabidopsis eli1 mutant shows discontinuous xylem strands (17). Isolation and functional characterization of these genes will be important for further dissection of the molecular mechanisms underlying xylem cell differentiation (Table 1). So far, no mutants with a complete block of xylem cell differentiation have been isolated presumably because these kinds of mutants are lethal. This greatly hinders the utilization of the genetic approach to study xylogenesis. One complementary approach is to use the zinnia in vitro tracheary element induction system to isolate genes associated with xylogenesis. Because isolated zinnia mesophyll cells can be induced to transdifferentiate into tracheary elements, this system has long been exploited to isolate genes involved in different stages of xylogenesis (34). Many genes that are induced within hours after hormonal treatment have been isolated in the zinnia system using PCR-amplied fragment length polymorphisms (61). Researchers anticipate that homologous genes will be found in Arabidopsis and their functions in xylogenesis studied by using T-DNA or transposon knock-out mutants.
TABLE 1 Mutants affecting vascular differentiation
Mutant wilted wilty-dwarf Species Maize Tomato Vascular phenotype Disrupted metaxylem differentiation Compound perforation plate in vessels instead of wild-type simple perforation plate Block of procambial cell division Misaligned vessel elements Increased size of vascular bundles in stems Reduced secondary xylem differentiation in stems Discontinuous xylem strands Reduced secondary wall formation in xylem cells Reduced secondary wall formation in xylem cells Reduced secondary wall formation in xylem cells Gapped xylem Reduced length of vascular cells Gene product Unknown Unknown Reference 68 1, 72

wol mp pin1 i1 eli1 irx1 irx2 irx3 gpx fra2

Arabidopsis Arabidopsis Arabidopsis Arabidopsis Arabidopsis Arabidopsis Arabidopsis Arabidopsis Arabidopsis Arabidopsis

Cytokinin receptor Auxin response factor Auxin efux carrier Homeodomain leucine zipper protein Unknown Cellulose synthase catalytic subunit Unknown Cellulose synthase catalytic subunit Unknown Katanin-like microtubule severing protein

47, 55, 81 10, 41 36, 67 105 17 87, 92 92 88, 92 91 15

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Cell Elongation
After initiation of vascular cell differentiation, the conducting cells, tracheary elements in the xylem and sieve elements in the phloem, undergo signicant elongation before the tubular conducting system is formed. Because developing conducting cells cease to elongate when the secondary cell wall starts to be laid down (1), which is typical of diffuse cell elongation, the molecular mechanisms regulating the elongation of conducting cells are likely similar to those for other nonvascular cells. A katanin-like microtubule-severing protein AtKTN1 is important for the normal elongation of both xylem and phloem cells (15), indicating that microtubules regulate cell elongation in vascular tissues. Microtubules are thought to direct the orientation of cellulose microbril deposition, which in turn determines the axis of cell elongation. Cell elonagtion requires the loosening of the existing cellulose-hemicellulose network, a process mediated by cell wall loosening enzymes such as expansins (22). Expansin mRNA is preferentially localized at the ends of differentiating tracheary elements in zinnia, suggesting that expansins are important in the elongation of vessel cells (46). Plant hormones are clearly involved in regulation of vascular cell elongation. Mutation of genes involved in brassinosteroid biosynthesis results in a dramatic reduction in length of all cells including vascular cells (20).

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Secondary Wall Thickening

After elongation, tracheary elements undergo secondary wall thickening with annular, helical, reticulate, scalariform, and pitted patterns (58). The thickened secondary wall provides mechanical strength to the vessels for withstanding the negative pressure generated through transpiration. The patterned secondary wall thickening is regulated through controlled deposition of cellulose microbrils, a process that is apparently regulated by the patterns of cortical microtubules located underneath the plasma membrane. Pharmacological studies have shown that disruption of the cortical microtubule organization completely alters the patterns of secondary wall thickening (3032). Little is known about how the cortical microtubules form different patterns and how they regulate the patterns of secondary wall thickening. In addition to cortical microtubules, microlaments also appear to be important for the normal patterning of secondary wall in tracheary elements (51). There has been a signicant progress in the characterization of genes involved in the synthesis of secondary wall, including synthesis of cellulose and lignin. Several Arabidopsis mutants affecting secondary wall formation have been isolated (91, 92); two of which encode cellulose synthase catalytic subunits that are specifically involved in cellulose synthesis in the secondary wall (87, 88). Isolation of these genes will further expand our understanding of secondary wall biosynthesis. Lignin impregnated in the cellulose and hemicellulose network provides additional mechanical strength to the secondary wall and also renders the secondary wall waterproof owing to its hydrophobic nature. Monolignols are synthesized

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through the phenylpropanoid pathway and are exported into the secondary wall where they are polymerized into lignin polymers. Most genes involved in monolignol biosynthesis have been isolated and characterized, and readers are referred to a recent review on this topic (97).

Cell Death
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After fullling cellular activities necessary for building up a secondary wall, developing tracheary elements undergo cell death to remove their cellular contents, and in the case of vessel elements, their ends are perforated to form tubular columns called vessels. The ends of vessel elements can be perforated with a single hole, a pattern called simple perforation plate, or with more than one hole, a pattern called complex perforation plate (28). Perforation sites contain only the primary wall that is digested by cellulase during autolysis, whereas the secondary wall impregnated with lignin is resistant to cellulase attack. However, to date, no cellulase genes have been shown to be specically expressed at the late stages of xylogenesis. Perforation plate patterns, whether simple or complex, are controlled by the patterned deposition of secondary wall on both ends of vessel elements. It is extremely interesting to note that mutation of a gene in the tomato wilty-dwarf mutant (1a, 72) converts the wild-type simple perforation plate in vessels into a compound perforation plate (Figures 2c,d ). Isolation of the corresponding gene should shed new insight into the mechanisms controlling the patterned secondary wall deposition. Hydrolytic enzymes including cysteine proteases (8, 45, 65, 101, 102), serine proteases (8, 38, 101, 102), and nucleases (5, 89, 100) are highly induced during xylogenesis, and they are stored in vacuoles before autolysis occurs (35). Cell death is initiated by disruption of the vacuole membrane, resulting in release of hydrolytic enzymes into the cytosol (37, 38, 53, 65). One of the biochemical markers for the cell death of tracheary elements is the degradation of nuclear DNA that can be detected by terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling (37, 63). Little is known about what signals trigger the biosynthesis of a battery of hydrolytic enzymes and the nal disruption of vacuoles, except for a possible involvement of calcium inux and an extracellular serine protease in the initiation of cell death of tracheary elements (38).

VASCULAR PATTERN FORMATION Vascular Bundles

Vascular tissues, xylem and phloem, within a vascular bundle can be organized into distinctive patterns, such as collateral, amphivasal, and amphicribral bundles. Recent genetic analysis has begun to unravel the molecular mechanisms underlying vascular pattern formation. Studies from three mutants have revealed that the vascular tissue organization within the bundles is controlled by positional

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TABLE 2 Mutants affecting vascular tissue organization within vascular bundles

Mutant phan Species Antirrhinum Vascular phenotype Amphicribral vascular bundles in leaves instead of wild-type collateral vascular bundles Amphivasal vascular bundles in leaves instead of wild-type collateral vascular bundles Amphivasal vascular bundles in leaves and stems instead of wild-type collateral vascular bundles Gene product MYB transcription factor Reference 95, 96

phb-1d

Arabidopsis

Homeodomain leucine zipper protein Homeodomain leucine zipper protein

59, 60

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avb1

Arabidopsis

104

information (Table 2). In Arabidopsis leaves, vascular tissues within a bundle are organized as collateral, i.e., xylem is parallel to phloem. In the bundle, xylem is positioned next to the adaxial side of leaves, and phloem is positioned next to the abaxial side of leaves. The leaves of Arabidopsis phb-1d mutant, which exhibits a loss of abaxial characters, have amphivasal vascular bundles, i.e., xylem surrounds phloem (59). Similarly, in the leaves of the Arabidopsis avb1 mutant, which shows a partial loss of leaf polarity (R. Zhong & Z-H. Ye, unpublished observations), the collateral vascular bundles are transformed into amphivasal bundles (104). In contrast, in the leaves of the Antirrhinum phan mutant, which causes a loss of adaxial cell fate, the collateral vascular bundles are transformed into amphicribral bundles, i.e., phloem surrounds xylem (95). This suggests that, when the positional information that determines the normal placement of xylem is disrupted, xylem forms a circle around phloem by default, as seen in the phb-1d and avb1 mutants. Similarly, when the positional information that determines the normal placement of phloem is disrupted, phloem forms a circle around xylem by default, as seen in the phan mutant. This also indicates that similar positional information is utilized by plants to control leaf polarity and vascular tissue organization in leaves. The PHB (60) and AVB1 (R. Zhong & Z-H. Ye, unpublished observations) genes have been cloned, and they encode proteins belonging to a family of homeodomain leucine-zipper transcription factors. The PHAN gene encodes a MYB transcription factor (96). With the availability of these molecular tools, it will be possible to further investigate how these transcription factors regulate the positional signals that direct various organizations of vascular tissues. Because auxin and cytokinin are inducers of vascular differentiation, it is reasonable to propose that the positional information might regulate the positions of the hormonal ow that determine the formation of various vascular tissue organizations. In Arabidopsis inorescence stems, the vascular tissues within a bundle are also organized as collateral. In the bundle, xylem is positioned next to the center of stems, and phloem is positioned next to the periphery (Figure 1c). In the stems of the avb1 mutant, the normal collateral placement of xylem and phloem is disrupted, leading to formation of amphivasal vascular bundles with xylem

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surrounding phloem (104) (Figure 1d ). This suggests that leaves and stems might share the same molecular mechanisms in controlling the organization of vascular tissues.

Vascular Patterning at the Organ Level

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At the organ level, vascular tissues can be arranged in a variety of patterns. In primary stems and roots, vascular bundles can be organized as a single ring or in a scattered pattern. In stems and roots with secondary growth, vasculature can be organized as a single ring, multiple concentric rings, multiple separated rings, or multiple scattered bands (58). In leaves, vascular bundles, often called veins, form diverse patterns such as parallel and networked arrangements. The positions of the polar auxin ow may determine the pattern of vascular tissues at the organ level (77, 78). This proposal has been supported by both pharmacological and genetic studies in Arabidopsis. Alteration of auxin polar transport by auxin polar transport inhibitors (57, 83) and by mutation of genes affecting auxin polar transport (12, 57) dramatically alters the venation pattern in Arabidopsis leaves. With the identication of all putative auxin efux carriers in the Arabidopsis genome, it is now possible to further investigate the roles of these carriers in determining the vascular patterns in different organs. Genetic analysis has indicated that vascular patterns at the organ level are also regulated by positional information (Tables 3 and 4). Mutation of the Arabidopsis AVB1 gene not only transforms the collateral vascular bundles into amphivasal bundles, but also disrupts the ring-like organization of vascular bundles in stems (104). In the avb1 mutant, multiple bundles are branched into the pith, a pattern reminiscent of those seen in the monocot stems. This suggests that, when the positional information that determines the ring-like vascular organization is disrupted, additional vascular bundles are formed in pith by default, as seen in the avb1 mutant. It will be interesting to investigate the distribution patterns of auxin efux carriers in the avb1 mutant. The importance of positional information in regulating vascular patterning is also demonstrated by several organ polarity mutants such as the yabby (84) and ago1 (14) mutants. These mutants exhibit altered venation patterns in leaves. The YABBY genes encode putative transcription factors (84), and the AGO gene encodes a protein with unknown functions (14). A number of other mutants affecting vascular patterning have been isolated (Tables 3 and 4). Most of these mutants were isolated based on alterations of the

TABLE 3 Mutants affecting vascular patterns in stems and roots

Mutant avb1 lsn1 Species Arabidopsis Maize Vascular phenotype Disruption of the ring-like vascular bundle organization in stems Disorganization of vascular bundles in roots and scutellar nodes Gene product Homeodomain leucine zipper protein Unknown Reference 104 54

196

YE TABLE 4 Mutants affecting leaf venation patterns

Mutant midribless mbl lop1 Species Pearl millet Arabidopsis Vascular phenotype Lack of midrib Gene product Unknown Unknown Reference 70 33 19

Panicum maximum Lack of midrib

Midvein bifurcation, Unknown discontinuous and reduced number of veins Discontinuous and reduced number of veins Discontinuous and reduced number of veins Reduced number of veins Reduced number of veins Discontinuous and reduced number of veins Discontinuous and reduced number of veins Discontinuous and reduced number of veins Discontinuous and reduced number of veins Discontinuous and reduced number of veins Reduced number of veins Reduced number of veins and free-ending vascular strands Exess of hydathodes Reduced number of veins Reduced number of veins Auxin response factor Unknown

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mp bdl ago l-5 yab3-1 cvp1, cvp2

Arabidopsis Arabidopsis Arabidopsis Arabidopsis Arabidopsis

10, 41 40

Protein with unknown 14 identity Transcription factors Unknown Unknown 84 18 52

van1, van2 Arabidopsis van3, van4 van5, van6 gnom/van7 sfc axr6 hve ixa Arabidopsis Arabidopsis Arabidopsis Arabidopsis Arabidopsis

Guanine-nucleotide exchange factor Unknown Unknown Unknown Unknown

52, 85 24 43 16 16

ehy pin1 i1

Arabidopsis Arabidopsis Arabidopsis

Unknown Auxin efux carrier

16 12

Homeodomain leucine 105 zipper protein

venation pattern in cotyledons or leaves. These mutations cause discontinuous, random, or reduced numbers of veins (16, 18, 24, 33, 52, 70). Recently, a maize mutant with an alteration of vascular patterns in roots and scutellar nodes has been described (54). All these vascular pattern mutants also display defects in other aspects of plant growth and development, indicating that the genes affected are involved in multiple processes important for normal plant development. Isolation of the corresponding genes in these mutants and further characterization of their functions will undoubtedly contribute to the dissection of pathways involved in vascular pattern formation.

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CONCLUSIONS
Signicant progress has been made in our understanding of vascular differentiation and pattern formation, which lays a foundation for further dissecting these complicated processes at the molecular level. The isolation of genes involved in auxin polar transport and signaling of auxin and cytokinin will help us to investigate how auxin polar ow is spatially regulated and how auxin and cytokinin signals are transduced to induce vascular differentiation. With the availability of many vascular pattern mutants and further characterization of their corresponding genes, it will soon be possible to investigate how positional signals determine the organization of vascular tissues. Although the zinnia system will still be an important player in the search for genes specically involved in tracheary element formation, the model plant Arabidopsis is undoubtedly a powerful genetic system for investigating the molecular mechanisms regulating different aspects of vascular differentiation and pattern formation. Because the inorescence stems and roots of Arabidopsis undergo secondary growth, Arabidopsis is also a useful genetic tool for studying wood formation. It is anticipated that a combined application of molecular, genetic, genomic, cellular, and physiological tools will soon lead to many exciting discoveries regarding the molecular mechanisms underlying vascular tissue differentiation and vascular tissue patterning. ACKNOWLEDGMENTS Work in the authors laboratory was supported by a grant from the Cooperative State Research, Education, and Extension Service, U.S. Department of Agriculture.
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Figure 1 Anatomy of vascular tissues. (a) Longitudinal section of an Arabidopsis stem showing vessels (arrow). (b) Tracheary elements differentiated from isolated zinnia mesophyll cells. (c) Cross section of the wild-type Arabidopsis stem showing a collateral vascular bundle. (d ) Cross section of the Arabidopsis avb1 mutant stem showing an amphivasal vascular bundle. ph, phloem; x, xylem. Figures 1c and d were reproduced with permission from (104).

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Figure 2 Anatomical phenotypes of two vascular mutants. (a) Cross section of the wild-type maize stem showing two prominent metaxylem cells (arrows) in a vascular bundle. x, protoxylem. (b) Cross section of the maize wilted mutant stem showing the absence of metaxylem cells in a vascular bundle. (c) Cross section of the wild-type tomato stem showing the simple perforation plate (arrow) in a vessel. (d ) Cross section of the tomato wilty-dwarf mutant showing a compound perforation plate (arrow) in a vessel. Figures 2a and b were reproduced with permission from (68). Figures 2c and d were reproduced with permission from (1).

Annual Review of Plant Biology Volume 53, 2002

CONTENTS
Annu. Rev. Plant Biol. 2002.53:183-202. Downloaded from arjournals.annualreviews.org by Michigan Technological University - J. R. VAN PELT LIBRARY on 11/11/07. For personal use only.

FrontispieceA. A. Benson PAVING THE PATH, A. A. Benson NEW INSIGHTS INTO THE REGULATION AND FUNCTIONAL SIGNIFICANCE OF LYSINE METABOLISM IN PLANTS, Gad Galili SHOOT AND FLORAL MERISTEM MAINTENANCE IN ARABIDOPSIS,
Jennifer C. Fletcher

xii 1 27 45 67 109 131

NONSELECTIVE CATION CHANNELS IN PLANTS, Vadim Demidchik,

Romola Jane Davenport, and Mark Tester

REVEALING THE MOLECULAR SECRETS OF MARINE DIATOMS,

Angela Falciatore and Chris Bowler

ABSCISSION, DEHISCENCE, AND OTHER CELL SEPARATION PROCESSES,

Jeremy A. Roberts, Katherine A. Elliott, and Zinnia H. Gonzalez-Carranza

PHYTOCHELATINS AND METALLOTHIONEINS: ROLES IN HEAVY METAL DETOXIFICATION AND HOMEOSTASIS, Christopher Cobbett
and Peter Goldsbrough 159 183 203

VASCULAR TISSUE DIFFERENTIATION AND PATTERN FORMATION IN PLANTS, Zheng-Hua Ye LOCAL AND LONG-RANGE SIGNALING PATHWAYS REGULATING PLANT RESPONSES TO NITRATE, Brian G. Forde ACCLIMATIVE RESPONSE TO TEMPERATURE STRESS IN HIGHER PLANTS: APPROACHES OF GENE ENGINEERING FOR TEMPERATURE TOLERANCE, Koh Iba SALT AND DROUGHT STRESS SIGNAL TRANDUCTION IN PLANTS,
Jian-Kang Zhu

225 247 275 299

THE LIPOXYGENASE PATHWAY, Ivo Feussner and Claus Wasternack PLANT RESPONSES TO INSECT HERBIVORY: THE EMERGING MOLECULAR ANALYSIS, Andr Kessler and Ian T. Baldwin e PHYTOCHROMES CONTROL PHOTOMORPHOGENESIS BY DIFFERENTIALLY REGULATED, INTERACTING SIGNALING PATHWAYS IN HIGHER PLANTS, Ferenc Nagy and Eberhard Sch fer a

329

vi

CONTENTS

vii

THE COMPLEX FATE OF -KETOACIDS, Brian P. Mooney, Jan A. Miernyk,

and Douglas D. Randall

MOLECULAR GENETICS OF AUXIN SIGNALING, Ottoline Leyser RICE AS A MODEL FOR COMPARATIVE GENOMICS OF PLANTS,
Ko Shimamoto and Junko Kyozuka
Annu. Rev. Plant Biol. 2002.53:183-202. Downloaded from arjournals.annualreviews.org by Michigan Technological University - J. R. VAN PELT LIBRARY on 11/11/07. For personal use only.

357 377 399

ROOT GRAVITROPISM: AN EXPERIMENTAL TOOL TO INVESTIGATE BASIC CELLULAR AND MOLECULAR PROCESSES UNDERLYING MECHANOSENSING AND SIGNAL TRANSMISSION IN PLANTS,
K. Boonsirichai, C. Guan, R. Chen, and P. H. Masson 421

RUBISCO: STRUCTURE, REGULATORY INTERACTIONS, AND POSSIBILITIES FOR A BETTER ENZYME, Robert J. Spreitzer
and Michael E. Salvucci 449 477 503 523

A NEW MOSS GENETICS: TARGETED MUTAGENESIS IN PHYSCOMITRELLA PATENS, Didier G. Schaefer COMPLEX EVOLUTION OF PHOTOSYNTHESIS, Jin Xiong and Carl E. Bauer CHLORORESPIRATION, Gilles Peltier and Laurent Cournac STRUCTURE, DYNAMICS, AND ENERGETICS OF THE PRIMARY PHOTOCHEMISTRY OF PHOTOSYSTEM II OF OXYGENIC PHOTOSYNTHESIS, Bruce A. Diner and Fabrice Rappaport INDEXES
Subject Index Cumulative Index of Contributing Authors, Volumes 4353 Cumulative Index of Chapter Titles, Volumes 4353

551

581 611 616

ERRATA
An online log of corrections to Annual Review of Plant Biology chapters (if any, 1997 to the present) may be found at http://plant.annualreviews.org/