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Annu. Rev. Plant Biol. 2002. 53:183202DOI: 10.1146/annurev.arplant.53.100301.135245

Copyright c 2002 by Annual Reviews. All rights reserved

VASCULAR TISSUE DIFFERENTIATION ANDPATTERN FORMATION IN PLANTS

Zheng-Hua YeDepartment of Botany, University of Georgia, Athens, Georgia 30602;

e-mail: [email protected]

Key Words auxin, procambium, positional information, venation, xylem

s Abstract Vascular tissues, xylem and phloem, are differentiated from meristem-atic cells, procambium, and vascular cambium. Auxin and cytokinin have been consid-ered essential for vascular tissue differentiation; this is supported by recent molecularand genetic analyses. Xylogenesis has long been used as a model for study of celldifferentiation, and many genes involved in late stages of tracheary element formationhave been characterized. A number of mutants affecting vascular differentiation andpattern formation have been isolated in Arabidopsis. Studies of some of these mutantshave suggested that vascular tissue organization within the bundles and vascular pattern

formation at the organ level are regulated by positional information.

CONTENTS

INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184

VASCULAR TISSUES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184

VASCULAR PATTERNS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185

Vascular Tissue Organization Within a Vascular Bundle . . . . . . . . . . . . . . . . . . . . . 185

Vascular Tissue Organization at the Organ Level. . . . . . . . . . . . . . . . . . . . . . . . . . .

185MODEL SYSTEMS FOR STUDYING VASCULAR DEVELOPMENT . . . . . . . . . . 186

Coleus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 186

Zinnia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 186

Arabidopsis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187

APPROACHES USED FOR STUDYING

VASCULAR DEVELOPMENT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187

VISUALIZATION OF VASCULAR TISSUES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 188

PROCESSES OF VASCULAR DIFFERENTIATION . . . . . . . . . . . . . . . . . . . . . . . . . 188

Formation of Procambium and Vascular Cambium . . . . . . . . . . . . . . . . . . . . . . . . . 188

Initiation of Xylem Differentiation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

190Cell Elongation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192

Secondary Wall Thickening . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192

Cell Death . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193

VASCULAR PATTERN FORMATION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193

Vascular Bundles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193

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Vascular Patterning at the Organ Level . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 195

CONCLUSIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197

INTRODUCTION

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 primarystems 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 first briefly 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 ofvascular 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 trans-

ports 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 fibers. 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 fibers. Sieve elements of nonflowering plants are sieve

cells that are connected with each other through sieve areas. Sieve elements of

most flowering plants are sieve tube members that are connected through sieve

plates to form continuous columns (28, 58).

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VASCULAR TISSUE DIFFERENTIATION 185

Vascular tissues can be formed from two different meristematic tissues, pro-

cambium 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 procam-bium 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 pro-

duce tracheary elements and xylary fibers 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 vas-

cular 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 less-common vascular tissue organizations were also evolved in vascular plants. In some

monocot plants such as Acorus and Dracaena, phloem is surrounded by a con-

tinuous 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. Sim-

ilar 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 consid-

ered 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 anetwork 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 VASCULARDEVELOPMENT

Coleus

It is apparent that the complexity of vasculartissues andtheir organizations presents

a big challenge for studying the molecular mechanisms underlying vascular dif-

ferentiation and pattern formation. At the same time, vascular tissues represent a

model for understanding many aspects of fundamental biological questions regard-

ing cell specification, 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 vascularstudy 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, iso-

lated 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 bio-

chemical 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 tra-

cheary element differentiation, including cell specification, patterned secondary

wall thickening, and programmed cell death.

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Arabidopsis

With the introduction of the model plantArabidopsis as a genetic system for study-

ing plant growth and development, Arabidopsis has been adopted as a powerful

system for genetic dissection of vascular differentiation and pattern formation. Un-

like 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 ofArabidopsis mutants have opened new avenues

for understanding the molecular mechanisms regulating various aspects of vas-

cular 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 organiza-

tion 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.

APPROACHES USED FOR STUDYINGVASCULAR DEVELOPMENT

Vascular development has traditionally been studied using physiological, biochem-ical, 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 Ara-

bidopsis 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 sec-

ondary 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-amplified 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 de-

velopment. 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 two-

hybrid 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

Themost 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 ofArabidopsis, 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 ofleaf 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 lignified 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 tis-

sues. 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 vas-

cular differentiation. The promoter ofTED3 gene, which is specifically expressedin 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 vas-

cular differentiation are also complicated, and many genes may be involved in

vascular development. Because most of the research on vascular differentiationhas 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. Procambialcells 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 precur-

sor 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. Earlyphysiological 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 inArabidopsis mutants. Mutation of theMP 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 vasculardifferentiation. The PIN1 gene

encodes an auxin efflux carrier (36), and the GNOM gene encodes a membrane-associated 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). Mu-

tation of the WOL/CRE1 gene, which encodes a cytokinin receptor (47, 55), leads

to differentiation of all procambial cells into protoxylem (55, 81). Crossing ofwol

withfass, a mutant with supernumerary cell layers, shows that WOL is not essentialfor phloem and metaxylem formation, indicating that WOL is involved in promo-

tion 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 pro-

gression (22a,b). Recently, investigators have shown that an inositol phospholipidkinase, 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 transduc-

tion 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 asATHB8 (6)and

Oshox1 (80) are expressed in procambial cells, but their precise roles in procambialcell 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 inflorescence stems of the ifl1 mutants leads to a block of vascularcambium activity at the basal parts of stems (103, 105). The block of vascular cam-

bium activity in the ifl1 mutants is associated with reduced expression of auxin

efflux carriers PIN3 and PIN4 (106), suggesting important roles of polar auxin

flow in vascular cambium activity. Because many auxin efflux carrier homologues

have been identified in the Arabidopsis genome, it will be important to investi-

gate 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 ob-servations). Cytokinin is considered essential for the continuous division of vas-

cular 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

inArabidopsis. Dissection of the signaling transduction pathways of auxin and cy-

tokinin 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 final 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 cam-

bial 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 for-

mation (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 in-

volved in this process because mutation of the MP gene results in misaligned

xylem strands (41, 69). Many other auxin response factors have been identified

(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),andtheArabidopsis 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 differenti-

ation (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 isolategenes 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-amplified 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 Species Vascular phenotype Gene product Reference

wilted Maize Disrupted metaxylem differentiation Unknown 68

wilty-dwarf Tomato Compound perforation plate in Unknown 1, 72

vessels instead of wild-type simple

perforation plate

wol Arabidopsis Block of procambial cell division Cytokinin receptor 47, 55, 81

mp Arabidopsis Misaligned vessel elements Auxin response factor 10, 41

pin1 ArabidopsisIncreased size of vascular bundles Auxin efflux carrier 36, 67

in stems

ifl1 Arabidopsis Reduced secondary xylem Homeodomain leucine 105

differentiation in stems zipper protein

eli1 Arabidopsis Discontinuous xylem strands Unknown 17

irx1 Arabidopsis Reduced secondary wall formation Cellulose synthase 87, 92

in xylem cells catalytic subunit

irx2 Arabidopsis Reduced secondary wall formation Unknown 92

in xylem cellsirx3 Arabidopsis Reduced secondary wall formation Cellulose synthase 88, 92

in xylem cells catalytic subunit

gpx Arabidopsis Gapped xylem Unknown 91

fra2 ArabidopsisReduced length of vascular cells Katanin-like microtubule 15

severing protein

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Cell Elongation

After initiation of vascular cell differentiation, the conducting cells, tracheary ele-

ments in the xylem and sieve elements in the phloem, undergo significant elonga-

tion before the tubular conducting system is formed. Because developing conduct-

ing 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 micro-

tubules regulate cell elongation in vascular tissues. Microtubules are thought to

direct the orientation of cellulose microfibril deposition, which in turn determines

the axis of cell elongation. Cell elonagtion requires the loosening of the exist-

ing 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).

Secondary Wall ThickeningAfter 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 microfibrils, a

process that is apparently regulated by the patterns of cortical microtubules lo-

cated 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 mi-

crotubules form different patterns and how they regulate the patterns of secondary

wall thickening. In addition to cortical microtubules, microfilaments also appear

to be important for the normal patterning of secondary wall in tracheary elements

(51).

There has been a significant progress in the characterization of genes involved

in the synthesis of secondary wall, including synthesis of cellulose and lignin. Sev-

eral Arabidopsis mutants affecting secondary wall formation have been isolated

(91, 92); two of which encode cellulose synthase catalytic subunits that are specif-

ically 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 addi-

tional 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 mono-

lignol biosynthesis have been isolated and characterized, and readers are referred

to a recent review on this topic (97).

Cell Death

After fulfilling cellular activities necessary for building up a secondary wall, devel-

oping 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 primarywall that is digested by cellulase during autolysis, whereas the secondary wall

impregnated with lignin is resistant to cellulase attack. However, to date, no cel-

lulase genes have been shown to be specifically 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 secondarywall 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 abattery of hydrolytic enzymes and the final disruption of vacuoles, except for a

possible involvement of calcium influx 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 under-

lying 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


phan Antirrhinum Amphicribral vascular bundles MYB transcription factor 95, 96

in leaves instead of wild-type

collateral vascular bundles

phb-1d Arabidopsis Amphivasal vascular bundles Homeodomain leucine 59, 60

in leaves instead of wild-type zipper protein

collateral vascular bundles

avb1 Arabidopsis Amphivasal vascular bundles Homeodomain leucine 104

in leaves and stems instead of zipper protein

wild-type collateral vascular bundles

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 ofArabidopsis phb-1dmutant, which exhibits a

loss of abaxial characters, have amphivasal vascular bundles, i.e., xylem surrounds

phloem (59). Similarly, in the leaves of theArabidopsis 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 ofadaxial 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-1dand 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 uti-

lized 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 PHANgene encodes a MYB transcription

factor (96). With the availability of these molecular tools, it will be possible to fur-

ther 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 flow that determine the

formation of various vascular tissue organizations.

In Arabidopsis inflorescence stems, the vascular tissues within a bundle are

also organized as collateral. In the bundle, xylem is positioned next to the cen-

ter 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

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 flow 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 trans-

port inhibitors (57, 83) and by mutation of genes affecting auxin polar transport

(12, 57) dramatically alters the venation pattern in Arabidopsis leaves. With the

identification of all putative auxin efflux 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 posi-

tional information that determines the ring-like vascular organization is disrupted,

additional vascular bundles are formed in pith by default, as seen in the avb1 mu-

tant. It will be interesting to investigate the distribution patterns of auxin efflux

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


avb1 Arabidopsis Disruption of the ring-like vascular Homeodomain leucine 104

bundle organization in stems zipper protein

lsn1 Maize Disorganization of vascular Unknown 54

bundles in roots and scutellar nodes

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TABLE 4 Mutants affecting leaf venation patterns


midribless Pearl millet Lack of midrib Unknown 70

mbl Panicum maximum Lack of midrib Unknown 33

lop1 Arabidopsis Midvein bifurcation, Unknown 19

discontinuous and reduced

number of veins

mp Arabidopsis Discontinuous and reduced Auxin response factor 10, 41

number of veins

bdl Arabidopsis Discontinuous and reduced Unknown 40

number of veins

ago Arabidopsis Reduced number of veins Protein with unknown 14

identity

fil-5 yab3-1 Arabidopsis Reduced number of veins Transcription factors 84

cvp1, cvp2 Arabidopsis Discontinuous and reduced Unknown 18

number of veins

van1, van2 Arabidopsis Discontinuous and reduced Unknown 52

van3, van4 number of veins

van5, van6

gnom/van7 Arabidopsis Discontinuous and reduced Guanine-nucleotide 52, 85

number of veins exchange factor

sfc Arabidopsis Discontinuous and reduced Unknown 24number of veins

axr6 Arabidopsis Discontinuous and reduced Unknown 43

number of veins

hve Arabidopsis Reduced number of veins Unknown 16

ixa Arabidopsis Reduced number of veins Unknown 16

and free-ending vascular

strands

ehy Arabidopsis Exess of hydathodes Unknown 16

pin1 Arabidopsis Reduced number of veins Auxin efflux carrier 12ifl1 Arabidopsis Reduced number of veins 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

Significant progress has been made in our understanding of vascular differentia-

tion and pattern formation, which lays a foundation for further dissecting thesecomplicated processes at the molecular level. The isolation of genes involved in

auxin polar transport and signaling of auxin and cytokinin will help us to inves-

tigate how auxin polar flow 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 correspond-

ing 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 specifically involved in tracheary ele-

ment formation, the model plant Arabidopsis is undoubtedly a powerful geneticsystem for investigating the molecular mechanisms regulating different aspects

of vascular differentiation and pattern formation. Because the inflorescence stems

and roots ofArabidopsis undergo secondary growth, Arabidopsis is also a useful

genetic tool for studying wood formation. It is anticipated that a combined appli-

cation 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.

Visit the Annual Reviews home page at www.annualreviews.org

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ation in cultured Zinnia cells. Plant Cell

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Brassinosteroid levels increase drasticallyprior to morphogenesis of tracheary ele-

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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 dwere

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 wiltedmutant 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-dwarfmutant 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).

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Annual Review of Plant Biology

Volume 53, 2002

CONTENTS

FrontispieceA. A. Benson xii

PAVING THE PATH, A. A. Benson 1

NEW INSIGHTS INTO THE REGULATION AND FUNCTIONALSIGNIFICANCE OF LYSINE METABOLISM IN PLANTS, Gad Galili 27

SHOOT AND FLORAL MERISTEM MAINTENANCE IN ARABIDOPSIS,Jennifer C. Fletcher 45

NONSELECTIVE CATION CHANNELS IN PLANTS, Vadim Demidchik,Romola Jane Davenport, and Mark Tester 67

REVEALING THE MOLECULAR SECRETS OF MARINE DIATOMS,Angela Falciatore and Chris Bowler 109

ABSCISSION, DEHISCENCE, AND OTHER CELL SEPARATION PROCESSES,Jeremy A. Roberts, Katherine A. Elliott, and Zinnia H. Gonzalez-Carranza 131

PHYTOCHELATINS AND METALLOTHIONEINS: ROLES IN HEAVY METALDETOXIFICATION AND HOMEOSTASIS, Christopher Cobbettand Peter Goldsbrough 159

VASCULAR TISSUE DIFFERENTIATION AND PATTERN FORMATIONIN PLANTS, Zheng-Hua Ye 183

LOCAL AND LONG-RANGE SIGNALING PATHWAYS REGULATINGPLANT RESPONSES TO NITRATE, Brian G. Forde 203

ACCLIMATIVE RESPONSE TO TEMPERATURE STRESS IN HIGHERPLANTS: APPROACHES OF GENE ENGINEERING FOR TEMPERATURE

TOLERANCE, Koh Iba 225SALT AND DROUGHT STRESS SIGNAL TRANDUCTION IN PLANTS,

Jian-Kang Zhu 247

THE LIPOXYGENASE PATHWAY, Ivo Feussner and Claus Wasternack 275

PLANT RESPONSES TO INSECT HERBIVORY: THE EMERGINGMOLECULAR ANALYSIS, Andr e Kessler and Ian T. Baldwin 299

PHYTOCHROMES CONTROL PHOTOMORPHOGENESIS BYDIFFERENTIALLY REGULATED, INTERACTING SIGNALINGPATHWAYS IN HIGHER PLANTS, Ferenc Nagy and Eberhard Sch afer 329

vi

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CONTENTS vii

THE COMPLEX FATE OF -KETOACIDS, Brian P. Mooney, Jan A. Miernyk,and Douglas D. Randall 357

MOLECULAR GENETICS OF AUXIN SIGNALING, Ottoline Leyser 377

RICE AS A MODEL FOR COMPARATIVE GENOMICS OF PLANTS,Ko Shimamoto and Junko Kyozuka 399

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

RUBISCO: STRUCTURE, REGULATORY INTERACTIONS, ANDPOSSIBILITIES FOR A BETTER ENZYME, Robert J. Spreitzerand Michael E. Salvucci 449

A NEW MOSS GENETICS: TARGETED MUTAGENESIS INPHYSCOMITRELLA PATENS, Didier G. Schaefer 477

COMPLEX EVOLUTION OF PHOTOSYNTHESIS, Jin Xiong and Carl E. Bauer 503

CHLORORESPIRATION, Gilles Peltier and Laurent Cournac 523

STRUCTURE, DYNAMICS, AND ENERGETICS OF THE PRIMARYPHOTOCHEMISTRY OF PHOTOSYSTEM II OF OXYGENICPHOTOSYNTHESIS, Bruce A. Diner and Fabrice Rappaport 551

INDEXES

Subject Index 581Cumulative Index of Contributing Authors, Volumes 4353 611

Cumulative Index of Chapter Titles, Volumes 4353 616

ERRATAAn 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/

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