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10.1146/annurev.arplant.53.100301.135245
Annu. Rev. Plant Biol. 2002. 53:183–202
DOI: 10.1146/annurev.arplant.53.100301.135245
c 2002 by Annual Reviews. All rights reserved
Copyright °
VASCULAR TISSUE DIFFERENTIATION AND
PATTERN FORMATION IN PLANTS
Zheng-Hua Ye
Department of Botany, University of Georgia, Athens, Georgia 30602;
e-mail: [email protected]
Key Words auxin, procambium, positional information, venation, xylem
■ 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 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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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 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 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 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, 11–13, 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 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 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 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 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 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 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 specification, 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.
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-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 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 1–4), 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
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 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 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 specifically 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 efflux 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 inflorescence stems of the ifl1 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 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 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 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 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 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), 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-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
vessels instead of wild-type simple
perforation plate
Unknown
1, 72
wol
Arabidopsis
Block of procambial cell division
Cytokinin receptor
47, 55, 81
mp
Arabidopsis
Misaligned vessel elements
Auxin response factor
10, 41
pin1
Arabidopsis
Increased size of vascular bundles
in stems
Auxin efflux carrier
36, 67
ifl1
Arabidopsis
Reduced secondary xylem
differentiation in stems
Homeodomain leucine
zipper protein
105
eli1
Arabidopsis
Discontinuous xylem strands
Unknown
17
irx1
Arabidopsis
Reduced secondary wall formation
in xylem cells
Cellulose synthase
catalytic subunit
87, 92
irx2
Arabidopsis
Reduced secondary wall formation
in xylem cells
Unknown
92
irx3
Arabidopsis
Reduced secondary wall formation
in xylem cells
Cellulose synthase
catalytic subunit
88, 92
gpx
Arabidopsis
Gapped xylem
Unknown
91
fra2
Arabidopsis
Reduced length of vascular cells
Katanin-like microtubule
severing protein
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 significant 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 microfibril 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).
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 microfibrils, 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 (30–32). 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, 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. 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
After fulfilling 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 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 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 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 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
Species
Vascular phenotype
Gene product
Reference
phan
Antirrhinum
Amphicribral vascular bundles
in leaves instead of wild-type
collateral vascular bundles
MYB transcription factor
95, 96
phb-1d
Arabidopsis
Amphivasal vascular bundles
in leaves instead of wild-type
collateral vascular bundles
Homeodomain leucine
zipper protein
59, 60
avb1
Arabidopsis
Amphivasal vascular bundles
in leaves and stems instead of
wild-type collateral vascular bundles
Homeodomain leucine
zipper protein
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 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 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
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 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
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 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 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
Mutant
Species
Vascular phenotype
Gene product
Reference
avb1
Arabidopsis
Disruption of the ring-like vascular
bundle organization in stems
Homeodomain leucine
zipper protein
104
lsn1
Maize
Disorganization of vascular
bundles in roots and scutellar nodes
Unknown
54
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TABLE 4 Mutants affecting leaf venation patterns
Mutant
Species
Vascular phenotype
Gene product
Reference
midribless
Pearl millet
Lack of midrib
Unknown
70
mbl
Panicum maximum Lack of midrib
Unknown
33
lop1
Arabidopsis
Midvein bifurcation,
Unknown
discontinuous and reduced
number of veins
19
mp
Arabidopsis
Discontinuous and reduced
number of veins
Auxin response factor
10, 41
bdl
Arabidopsis
Discontinuous and reduced
number of veins
Unknown
40
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
number of veins
Unknown
18
van1, van2 Arabidopsis
van3, van4
van5, van6
Discontinuous and reduced
number of veins
Unknown
52
gnom/van7
Arabidopsis
Discontinuous and reduced
number of veins
Guanine-nucleotide
exchange factor
52, 85
sfc
Arabidopsis
Discontinuous and reduced
number of veins
Unknown
24
axr6
Arabidopsis
Discontinuous and reduced
number of veins
Unknown
43
hve
Arabidopsis
Reduced number of veins
Unknown
16
ixa
Arabidopsis
Reduced number of veins
and free-ending vascular
strands
Unknown
16
ehy
Arabidopsis
Exess of hydathodes
Unknown
16
pin1
Arabidopsis
Reduced number of veins
Auxin efflux carrier
12
ifl1
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 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 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 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 specifically 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 inflorescence 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 author’s 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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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).