Download The shoot apical meristem and development of vascular architecture1

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REVIEW / SYNTHÈSE
The shoot apical meristem and development of
vascular architecture1
Nancy G. Dengler
Abstract: The shoot apical meristem (SAM) functions to generate external architecture and internal tissue pattern as well
as to maintain a self-perpetuating population of stem-cell-like cells. The internal three-dimensional architecture of the vascular system corresponds closely to the external arrangement of lateral organs, or phyllotaxis. This paper reviews this correspondence for dicotyledonous plants in general and in Arabidopsis thaliana (L.) Heynh., specifically. Analysis is partly
based on the expression patterns of the class III homeodomain-leucine zipper transcription factor ARABIDOPSIS THALIANA HOMEOBOX GENE 8 (ATHB8), a marker of the procambial and preprocambial stages of vascular development, and
on the anatomical criteria for recognizing vascular tissue pattern. The close correspondence between phyllotaxis and vascular pattern present in mature tissues arises at early stages of development, at least by the first plastochron of leaf primordium outgrowth. Current literature provides an integrative model in which local variation in auxin concentration regulates
both primordium formation on the SAM and the first indications of a procambial prepattern in the position of primordium
leaf trace as well as in the elaboration of leaf vein pattern. The prospects for extending this model to the development of
the complex three-dimensional vascular architecture of the shoot are promising.
Key words: ATHB8, auxin, phyllotaxis, ATPIN1, procambium, vascular development.
Résumé : La fonction du méristème apical de la tige est de générer l’architecture externe et le patron histologique interne,
ainsi que de maintenir une population de cellules de nature caulinaire par auto-perpétuation. L’architecture interne tridimensionnelle du système vasculaire correspond étroitement à l’arrangement externe des organes latéraux, ou phyllotaxie.
L’auteur passe en revue cette correspondance chez les plantes dicotyles en général, et plus particulièrement chez l’Arabidopsis thaliana. L’analyse est partiellement basée sur l’expression des patrons de classe III du facteur de transcription de
l’homéodomaine-leucine-zipper, ARABIDOPSIS THALIANA HOMEOBOX GENE 8 (ATHB8), un marqueur des stades
cambial et procambial du développement vasculaire, ainsi que sur des critères anatomiques pour reconnaı̂tre le patron des
tissus vasculaires. L’étroite correspondance entre la phyllotaxie et le patron des tissus vasculaires, dans les tissus matures,
apparaı̂t à un stade précoce du développement, au moins au premier plastochron de l’apparition du primordium foliaire. La
littérature courante présente un modèle intégrateur dans lequel la variation locale des teneurs en auxines règle à la fois la
formation du primordium sur le méristème apical de la tige et les premières indications d’un pré-patron procambial, dans
la position de la trace foliaire du primordium, ainsi que dans l’élaboration du patron vasculaire foliaire. La perspective
d’étendre ce modèle de développement de l’architecture vasculaire tridimensionnelle complexe de la tige apparaı̂t prometteuse.
Mots clés : ATHB8, auxine, phyllotaxie, ATP1N1, procambium, développement vasculaire.
[Traduit par la Rédaction]
Introduction
The shoot apical meristem (SAM) functions to generate
external architecture and internal tissue pattern as well as to
maintain a self-perpetuating population of cells. Knowledge
of the development and behavior of the apical meristems is
Received 22 February 2006. Published on the NRC Research
Press Web site at http://canjbot.nrc.ca on 6 February 2007.
N.G. Dengler. Department of Botany, University of Toronto,
Toronto, ON M5S 1A1, Canada (e-mail:
[email protected]).
1This
review is one of a selection of papers published on the
Special Theme of Shoot Apical Meristems.
Can. J. Bot. 84: 1660–1671 (2006)
prerequisite for understanding plant development as well as
the special properties of plants as organisms with an indeterminate body plan. Recently, attention has focused on the
generation of external architecture, specifically the placement of lateral organs (e.g., Fleming 2005; Reinhardt 2005),
and on the formation and maintenance of the population of
stem-cell-like cells at the core of the SAM (e.g., Baurle and
Laux 2003; Carles and Fletcher 2003). Less attention has
been given to the generation of the pattern of dermal,
ground, and vascular tissues within the shoot. While the protoderm (precursor of the dermal tissue system) is derived
from the surface layer (L1) of the SAM simply by a restriction of division plane to anticlinal, the gradual emergence of
vascular pattern from more homogeneous-appearing precur-
doi:10.1139/B06-126
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sors derived from the L2 and deeper layers of the SAM is
less well understood (Steeves and Sussex 1989). The procambium (vascular tissue precursor) becomes distinct from
surrounding ground meristem (ground tissue precursor) by
differential patterns of cellular vacuolation, division, and enlargement (Esau 1965a, 1965b). Procambial pattern can be
recognized because the component cells are elongate in
shape and less vacuolated than adjacent ground meristem
and form continuous strands (Esau 1965a, 1965b; Nelson
and Dengler 1997). As it emerges, the procambial system
can be seen to form a complex, three-dimensional architecture within the shoot that is continuous with more mature
parts of the vascular system. Moreover, the complex internal
architecture of the vascular system corresponds closely to
the external architecture of lateral organ arrangement, or
phyllotaxis.
The purpose of this review is to examine the close correspondence between phyllotaxis and primary vascular architecture. The literature on this subject extends back for
almost 150 years, since botanists such as Nägeli (1858) and
DeBary (1884) noted that the geometric array of developing
and mature leaves gives an external clue to the internal arrangement of vascular bundles. In past decades, the causality
of this correspondence has been hotly debated, but as emphasized by Esau (1965a, 1965b), the opposing views that
either (i) new primordia induce the formation of the vascular
bundles that supply them or (ii) acropetal development of
vascular bundles induces the formation of primordia are
oversimplifications, and it is more likely that both phyllotaxis and vascular architecture are determined by a common
mechanism. Recent experimental and modeling studies have
provided strong evidence for such a common mechanism
(Fleming 2005; Reinhardt and Kuhlemeier 2002; Reinhardt
et al. 2003; Reinhardt 2005; Smith et al. 2006; Jönsson et
al. 2006). In this paper, I first review the expression pattern
of ARABIDOPSIS THALIANA HOMEOBOX GENE8
(ATHB8), a putative marker of procambium, and its precursors within the SAM region. Second, I review primary vascular architecture of dicotyledonous shoots and its
correspondence to phyllotaxis and then describe this correspondence for A. thaliana based on an analysis of procambium anatomy and the expression pattern of ATHB8
(based on the results of Kang et al. 2003). Third, I describe
developmental aspects of procambium pattern, including the
pattern of ATHB8 expression. Finally, I review a current
model for regulation of both phyllotaxis and its corresponding vascular architecture by active modulation of local auxin
concentration.
ATHB8 as a marker of primary vascular
development
The ARABIDOPSIS THALIANA HOMEOBOX GENE8
(ATHB8) is one of five members of a family of class III
homeodomain-leucine zipper (HD-Zip) transcription factors
in the Arabidopsis genome that functions in the formation
of meristems, in the dorsiventral patterning of lateral organs, and in the patterning and differentiation of vascular
tissues (McConnell et al. 2001; Emery et al. 2003; Floyd
and Bowman 2004). Four members of the family (REVOLUTA, PHABULOSA, PHAVOLUTA, and ATHB15/CO-
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RONA) are expressed in the SAM, adaxial domains of
lateral organs, and developing vascular tissues, while expression of ATHB8 is restricted to developing vascular tissues (Baima et al. 1995; McConnell et al. 2001; Emery et
al. 2003; Prigge et al. 2005; Williams et al. 2005). During
the development of leaf venation pattern, ATHB8-GUS is
expressed at very early stages in positions where veins are
predicted to appear, but before the diagnostic anatomical
features of procambium are expressed (Kang and Dengler
2004; Scarpella et al. 2004). In developing leaves, linearly
adjacent ground tissue cells initiate ATHB8 expression, and
development is continuous and polar in the sense that the
first cells to express ATHB8-GUS are adjacent to preexisting procambial strands and that ground cells at the
terminus of a developing file are recruited to the ATHB8GUS-expressing file, extending it across a panel of ground
tissue (Kang and Dengler 2004; Scarpella et al. 2004). This
expression pattern within the ground meristem presages the
anatomical emergence of procambium and has been termed
‘‘preprocambium’’ (Mattsson et al. 2003). Following the
preprocambial stage of development, cells in the file acquire the distinctive anatomical features of procambium,
and ATHB8-GUS expression increases (Kang and Dengler
2004; Scarpella et al. 2004). In contrast with the progressive appearance of the preprocambial phase, the emergence of procambium anatomy appears to occur
simultaneously along the file of cells (Scarpella et al.
2004). As xylem and phloem cells gradually differentiate
from procambial tissue, ATHB8-GUS expression becomes
restricted to the residual procambium between the vascular
tissues and undifferentiated cells on the adaxial (xylem)
side of procambial strands; expression ceases in fully differentiated veins (Kang and Dengler 2002). Similarly, in
stem vascular bundles, ATHB8 expression becomes restricted to a narrow zone of procambium between the differentiating xylem and phloem tissues (Baima et al. 1995).
Thus, ATHB8 expression provides a uniquely suitable
marker for analysis of vascular architecture, as it defines
both an early prepattern and procambium itself throughout
its development.
Despite this distinctive expression pattern, the specific
developmental function of ATHB8 is unknown (Emery et
al. 2003; Prigge et al. 2005). Homozygous ATHB8 loss-offunction mutants have no detectable phenotype (Baima et
al. 2001), while ectopic expression of ATHB8 results in proliferation of xylem precursor cells and subsequent increase
in the numbers of mature xylem cells (Baima et al. 2001).
In contrast, single loss- or gain-of-function mutations in
other members of the class III HD-Zip gene family result
in dramatic conversions of vegetative and floral lateral organ dorsiventral symmetry (McConnell et al. 2001; Emery
et al. 2003; Prigge et al. 2005). Mutants of ATHB8 also
have relatively little effect other than smaller stature in triple, quadruple, and quintuple combinations with other class
III HD-Zip mutants (Prigge et al. 2005). There is some evidence, however, that ATHB8 may interact antagonistically
with the REVOLUTA and ATHB15/CORONA loci as defects
in the differentiation of sclerenchyma fibers from the
ground tissue in inflorescence stems normally associated
with these mutants are suppressed in triple mutants (Prigge
et al. 2005). Members of the class III HD-Zip gene family
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clearly have overlapping and redundant functions in meristem establishment, organ polarity, and vascular development, making it difficult to establish the functions of a
single member such as ATHB8 through mutant analysis.
Evidence of a function for ATHB8 in vascular patterning
and development comes from observations of ATHB8 expression in response to the plant growth hormone auxin.
ATHB8-GUS expression is upregulated in response to auxin
treatment in wounded tobacco stems (Baima et al. 1995),
and ATHB8 mRNA increases in Arabidopsis whole seedlings or detached leaves incubated with auxin (Baima et al.
1995; Mattsson et al. 2003). Additionally, ATHB8 transcript
levels are reduced when the auxin response factor MONOPTEROS is impaired or are increased when MONOPTEROS is
overexpressed (Mattsson et al. 2003). GUS expression
driven by the synthetic auxin response element DR5 marks
the preprocambial stage of leaf vein development (Mattsson
et al. 2003), as does ATHB8-GUS (Kang and Dengler 2004;
Scarpella et al. 2004). These observations indicate that
ATHB8 expression might represent a downstream event in
the process that translates an auxin signal into a procambial
strand. The canalized flow of auxin through shoot tissues is
hypothesized to be the specific signal that induces formation
of a vascular strand (Sachs 1981, 1991). Support for this
model comes from experiments demonstrating that an artificial auxin source can induce the formation of a vascular
strand within wounded stem tissue (reviewed in Sachs
1981; Lyndon 1990). Numerous physiological experiments
have shown that auxin moves basipetally within intact stems
(reviewed in Lomax et al. 1995) and that movement is dependent on the cellular localization of a plasma membranebound protein ARABIDOPSIS THALIANA PIN-FORMED
1 (ATPIN1) (reviewed in Paponov et al. 2005). ATPIN1 is
one of eight PIN genes present in the Arabidopsis genome
(Paponov et al. 2005). The encoded PIN proteins have been
shown to be required for normal plant embryogenesis, organogenesis, phototropism, and gravitropism and are thought
to act through a role in polar auxin transport, although it is
currently unknown whether they act as auxin efflux carriers
directly or as regulators of polar auxin transport (Paponov et
al. 2005). Nevertheless, polar auxin movement is dependent
on the polar localization of ATPIN1 protein within the cell
(Galweiler et al. 1998; Benková et al. 2003).
The developmental responses to polar auxin movement
and signaling are not simple, as a complex series of coordinated cell divisions, cell enlargement, and patterned differentiation events are required to produce the highly
organized and functional vascular strand rather than a broad
unpatterned zone of vascular cells (Berleth and Mattsson
2000; Berleth et al. 2000). A role for ATHB8 in this process
is still a putative one, but one that we have exploited for a
characterization of primary vascular architecture in the compressed, miniature shoot of Arabidopsis.
Phyllotaxis and shoot vascular architecture
The pattern of initiation of leaf primordia on the flanks of
the SAM gives rise to one of the most conspicuous features
of whole-shoot morphology, phyllotaxis. Phyllotactic patterns generally are regular (although exceptions occur: Kelly
and Cooke 2003; Jeune and Barabé 2004), and individual
Can. J. Bot. Vol. 84, 2006
species or whole taxonomic groups are characterized by specific patterns, usually helical, distichous, decussate, or
whorled. Developmental shifts in phyllotaxis may occur,
such as those associated with shoot phase change from juvenile to adult or from vegetative to reproductive (Poethig
1990; Kwiatkowska 1995). Helical phyllotaxis is the most
common pattern among dicotyledons and has received the
most attention in terms of analysis of the geometrical patterns and modeling pattern generation within the SAM
(Richards 1951; Mitchison 1977; Steeves and Sussex 1989;
Lyndon 1990, 1998; Jean 1994; Adler et al. 1997; Reinhardt
and Kuhlemeier 2002; Smith et al. 2006; Jönsson et al.
2006). In species with helical phyllotaxis, leaf primordia are
initiated at a more or less constant divergence angle (approximately 137.58) along a shallow helix, the ontogenetic
(or ‘‘genetic’’) helix. Additional helices that are steeper
than the ontogenetic helix, the parastichies, can be recognized on the exterior of the shoot and, more readily, in
transverse sections of the shoot apex region (Esau 1965a,
1965b; Beck et al. 1982; Kirchoff 1984) (Fig. 1A). Leaf
primordia that are in direct contact form conspicuous contact parastichies, while steeper noncontact parastichies can
also be recognized (Kirchoff 1984). The serial positions of
leaves within a parastichy as well as the numbers of clockwise and anticlockwise parastichies are integers belonging to
the Fibonacci summation series (Richards 1951; Mitchison
1977; Esau 1965a, 1965b). Knowledge of specific parameters
of a helical phyllotactic system makes it possible to predict
the position of the next leaf primordium to be initiated on
the flanks of the SAM with considerable accuracy.
Similarly, knowledge of phyllotaxis permits predictions
about the placement of vascular bundles within the stem
(Girolami 1953; Skipworth 1962; Philipson and Balfour
1963; Esau 1965a, 1965b; Beck et al. 1982; Kirchoff 1984).
The longitudinal vascular bundles of the stem (here referred
to as vascular sympodia and most clearly recognizable in
immature portions of the stem) branch at intervals to give
rise to the leaf traces, the individual smaller vascular bundles that supply the leaves. The number of vascular sympodia usually reflects phyllotaxis: for instance, plants with
distichous or decussate phyllotaxis typically have even numbers of vascular sympodia (e.g., 4, 6), while plants with helical phyllotaxis have a number of sympodia belonging to the
Fibonacci summation series (e.g., 5, 8, 13: Beck et al. 1982;
Kirchoff 1984). In species with a single trace supplying each
leaf (the common condition: Esau 1965a, 1965b; Beck et al.
1982), leaves belonging to one parastichy all derive their
traces from the same vascular sympodium. In species with
three or more traces per leaf, the central traces are supplied
from the same vascular sympodium, while the lateral traces
are derived from adjacent sympodia (e.g., Larson 1975). In
some species, there are no interconnections between adjacent vascular sympodia (an open pattern), so that each vascular sympodium extends in a steep helix that mirrors one
parastichy on the exterior of the stem and branches to give
rise to leaf traces at regular intervals. This simple, open pattern gives rise to the sectoriality observed in some studies of
long-distance transport of water, solutes, and signaling molecules (Marshall 1996; Orians and Jones 2001). In other species, regular anastomoses between vascular sympodia form a
closed, reticulate pattern in which leaf traces are derived as
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Fig. 1. Phyllotaxis and primary vascular architecture in a vegetative shoot of Arabidopsis. (A) Cross section at the level of the shoot apical
meristem. Rosette leaves are numbered according to order of ontogenetic helix. The n + 3 and n + 5 contact parastichies are indicated, as
are the steeper n + 8 and n + 13 noncontact parastichies. (B) Cross section at 66 mm below the shoot apical meristem. Vascular bundles
represent either individual leaf traces (3, 4, 5, 6, 7) or vascular sympodia that will give rise to multiple leaf traces (8, 9, 10, 11, 12). Solid
lines, clockwise parastichies; broken lines, anticlockwise parastichies. Scale bar = 50 mm. (From Kang et al. 2003, reproduced with permission of the New Phytol. 158: 53–64).
branches of two adjacent vascular sympodia. Interestingly, a
correlation between the relative timing of the onset of cambial activity and the nature of the vascular system has been
noted in a modest species sample: secondary vascular development is initiated early when primary vascular architecture
is open, but initiated late and (or) is limited in extent when
primary vascular architecture is closed (Dormer 1945, 1946;
Philipson and Balfour 1963).
Primary vascular architecture in Arabidopsis:
mature pattern
Vegetative rosette
Based on analysis of the patterns of ATHB8-GUS expression and of anatomically defined procambium and (or) vascular tissues, vascular architecture of the vegetative rosette
of Arabidopsis is a closed, reticulate pattern that corresponds
closely to phyllotaxis (Figs. 1 and 2) (see Kang et al. 2003).
In vegetatively growing shoots with 20 or more leaves, the
most conspicuous contact parastichies are those connecting
every third leaf (n + 3) and every fifth leaf (n + 5) of the
ontogenetic helix (Fig. 1A). These contact parastichies extend up the shoot axis in either a clockwise or a counterclockwise direction (n + 5 and n + 3, respectively, in
Fig. 1A), depending on the overall orientation of shoot helical
phyllotaxis (anticlockwise for the shoot illustrated in
Fig. 1A). Individual rosettes with clockwise or anticlockwise
helical phyllotaxis occur with approximately equal frequencies in Arabidopsis (Kang et al. 2003). Generally, three n + 3
contact parastichies (connecting leaves 7, 10, 13, 16, etc.,
leaves 5, 8, 11, 14, etc., leaves 6, 9, 12, 15, etc.) and five
n + 5 contact parastichies (connecting leaves 5, 10, 15,
etc., leaves 6, 11, 16, etc., leaves 7, 12, 17, etc., leaves 8,
13, 18, etc., leaves 9, 14, 19, etc.) are present. In addition
to these more obvious contact parastichies, steeper, noncontact parastichies (n + 8, n + 13; Fig. 1A) can be superimposed on overall shoot helical phyllotaxis. Geometrical
properties such as these intersecting parastichies and other
properties of leaf arrangement accurately predict the spatial
positioning of vascular bundles within the stem.
The vascular bundles seen in any one cross section of the
stem represent either individual leaf traces (4 in Fig. 1B) or
the vascular sympodia that branch and give rise to the individual leaf traces (e.g., branches from the sympodium labeled 9 in Fig. 1B give rise to the traces of leaves 9, 14,
and 17). The levels of branching of parent sympodia and
the divergence of leaf traces determine the number of vascular strands observed in individual transverse sections, but the
number in wild-type Arabidopsis is typically eight (Fig. 1B).
When individual vacular bundles are traced through successive serial sections, they can be seen to branch and give rise
to the traces of leaves that are positionally related in the n +
8 and n + 5 parastichies. For instance, the sympodium supplying leaf 12 is derived from branches of bundles supplying
leaf 4 (antecedent in n + 8 parastichy) and leaf 7 (antecedent
in n + 5 parastichy) (Fig. 2), forming an anastomosing pattern and the closed pattern of primary vascular architecture
that characterizes Arabidopsis vegetative growth (Fig. 2).
Thus, vascular architecture of the Arabidopsis shoot is a
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Fig. 2. Idealized two-dimensional diagram representing primary vascular architecture in vegetative shoots of Arabidopsis. Foliage leaves
are represented by squares, numbered according to ontogenetic helix. Squares represent the approximate level of the leaf base. Leaf traces
are derived as branches of vascular sympodia supplying antecedent leaves in the n + 8 (blue) and n + 5 (green) parastichies, a pattern
established only after the second leaf in each n + 8 parastichy. Leaf traces are detectable during P1 (leaf 19) as branches from the antecedent leaf trace/sympodium in the n + 8 parastichy, while the n + 5 connections are present 3–4 plastochrons later (leaf 16). Branches connecting sympodia are shown as horizontal, reflecting the vertically compressed architecture of the rosette. Vascular bundles connected to
antecedent sympodia are illustrated as double cylinders, although they are anatomical coherent (see Fig. 1B); those connected to one antecedent sympodium are illustrated as one. The blue line at the base of the illustration represents the solid cylinder of the hypocotyl vasculature, which gives rise directly to cotyledonary and juvenile leaf traces (see Busse and Evert 1999). Not to scale.
highly integrated system in which the vascular supply to
each leaf is directly connected to antecedent leaves in two
different parastichies, providing alternative pathways for the
long-distance movement of water and solutes.
Although the fully expressed primary vascular architecture is a closed, reticulate system, the formation of the anastomosing procambial strands is not synchronous in that the
vascular connection with the n + 5 antecedent leaf lags behind the n + 8 connection during development. When a leaf
trace is first detectable, it extends as a branch of the trace of
its n + 8 antecedent leaf and terminates just below its corresponding primordium within the SAM (see Kang et al.
2003). Connections with the n + 5 antecedent leaf trace are
formed three to four plastochrons later; thus, on a developmental basis, shoot primary vascular architecture is initially
an open system but quickly becomes modified as a closed
reticulum (summarized in Fig. 2).
The closed, reticulate pattern of vascular architecture with
regular connections between the sympodia corresponding to
the n + 5 and n + 8 parastichies characterizes the adult
phase of shoot ontogeny. During the juvenile phase, however, phyllotaxis is subdecussate, and the traces to leaves 1
to 4 arise directly from the vascular cylinder of the hypocotyls, as do those of the cotyledons (see Busse and Evert
1999; Kang et al. 2003) (Fig. 2). Branches from these traces
anastomose to form the traces of the first-formed adult
leaves, and connections are initially between the sympodia
corresponding to the n + 3 and n + 5 parastichies. The for-
mation of leaf 9, which establishes the first n + 8 parastichy,
initiates the fully expressed pattern summarized in Fig. 2.
Inflorescence
Upon the induction of reproductive growth, the SAM initiates floral meristems in place of leaves along the ontogenetic helix of the vegetative rosette (Fig. 3). In Arabidopsis
plants grown under long-day inductive conditions, floral
meristems are first formed at position 10, 11, or 12 (12 in
Fig. 3A and 10 in Fig. 4; see Kang et al. 2003). At first, the
vascular architecture of the inflorescence extends the reticulate pattern of the vegetative rosette, with floral meristem
traces derived from those of the antecedent organs in the
n + 8 and n + 5 parastichies. For instance, in the inflorescence illustrated in Fig. 4, the sympodium supplying flower
12 is derived from those supplying leaves 4 (n + 8 parastichy) and 7 (n + 5 parastichy). After formation of the second flower in each n + 5 parastichy, however, vascular
architecture switches to an open pattern, with primary connections along the n + 5 parastichies (e.g., flower 17,
Fig. 4). Although the basic pattern follows that of the vegetative rosette, the inflorescence pattern differs in two specific ways: (i) the flower trace connects with the trace/
sympodium corresponding to the n + 5, not the n + 8 parastichy, and (ii) a second connection with the adjacent sympodium was not detected, resulting in a primarily open
pattern of inflorescence vascular architecture (summarized
in Fig. 4). ATHB8-GUS expression within new procambial
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Fig. 3. Phyllotaxis and primary vascular architecture in the inflorescence of Arabidopsis. (A) Cross section at the level of the shoot apical
meristem. Rosette leaves (5–8), cauline leaves (9–11), and floral meristems (12–21) are numbered in order of formation on the ontogenetic
helix. The n + 3 and n + 5 contact parastichies are indicated, as are the steeper n + 8 and n + 13 noncontact parastichies. (B) Cross section
at 490 mm below the shoot apical meristem. Rosette leaves 5–8 and the trace/sympodia supplying cauline leaves 9–11 and flowers 12–15 are
numbered. Note the axillary buds associated with rosette leaves 5–8 and axillary bud leaf primordia (arrows). Scale bar = 50 mm. (From
Kang et al. 2003, reproduced with permission of the New Phytol. 158: 53–64).
strands is weaker in the inflorescence apex than in vegetative apices, but the timing in relation to primordium formation and the longitudinal pattern of ATHB8-GUS expression
appears to be similar (Kang et al. 2003).
Although inflorescence vascular architecture is initially an
open system, secondary modifications reinstate the closed
reticulate nature of the shoot’s primary vascular architecture.
Accessory traces form bridges between individual flower
bud traces and the adjacent n + 3 and n + 5 sympodia
(Fig. 4). Such accessory traces are formed relatively late
(usually 10 or more plastochrons after floral meristem initiation), are narrow in diameter relative to the floral meristem
traces, and have a horizontal course.
Axillary buds
Upon transition from the vegetative to the reproductive
phase, axillary buds are initiated basipetally, starting with
the cauline leaves (Long and Barton 2000). Axillary bud
meristems initially lack detectable vascular bundles, but the
appearance of two short procambial strands is coincident
with formation of the first two leaf primordia on the axillary
shoot (see Kang et al. 2003). These procambial strands are
not isolated but appear to be continuous as branches of either the leaf trace alone (most rosette leaves) or the adjacent
vascular sympodia (cauline leaves) or a combination of the
two patterns (summarized in Fig. 4; Kang et al. 2003).
Thus, the vascular connections for the primary inflorescence
branches associated with the cauline leaves are well integrated with at least three vascular sympodia, providing a
built-in redundancy of vascular pathways supplying the
flowers and developing siliques born on those branches if
individual vascular bundles are damaged.
The stepwise elaboration of the primary vascular system
in vegetative and reproductive shoots of Arabidopsis involves the SAM itself as well as older regions of the stem.
Formation of the leaf trace (derived from the n + 8 sympodium) occurs during the first plastochron (P1), while the
connection with the n + 5 sympodium occurs later (P3 or
P4). Vascular connections between axillary buds and adjacent vascular sympodia develop outside the SAM in older
tissues (depending on growth conditions), as do those that
connect the traces of developing flower buds with adjacent
sympodia. These later developmental events are superimposed on the initial primary pattern and presumably require
comparable developmental signals and signaling pathways,
although the developmental environment in terms of overall
tissue differentiation differs from that within the SAM. The
progressive elaboration of the primary vascular system allows plants to respond appropriately to variation in the
growth environment in that the pattern may be arrested at a
simple phase when plants are short-lived or elaborated when
growth is prolonged. Under some growth conditions, secondary vascular development occurs within the rosette and the
basal portion of the inflorescence axis (Altamura et al. 2001;
Chaffey et al. 2002), replacing the primary vascular system
functionally.
The basic features of vascular development described for
the rosette plant Arabidopsis on the basis of ATHB8-GUS
expression correspond to descriptions of elongate shoots in
other species studied, most notably for Linum usitatissimum
L. (Linaceae) (Girolami 1953), Hectorella caespitosa
J.D. Hooker (Portulaceae) (Skipworth 1962), and Populus
deltoides Bartr. ex Marsh. (Saliceae) (Larson 1975). In herbaceous Linum and Hectorella, primary vascular architecture
is a closed, reticulate system with single acropetally developing leaf traces connected to vascular sympodia that correspond to parastichies. As these shoots mature, the numbers
of parastichies (and the numbers of intervening leaves along
a parastichy: n + 13, n + 21, etc.) and vascular sympodia increase, just as seen for the juvenile to adult transitions in
Arabidopsis. In woody Populus, vascular architecture is a
more complex, open system with three traces per leaf, yet
procambial strands develop acropetally and precisely according to phyllotaxis (Larson 1975, 1977). In Populus, vas#
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Fig. 4. Idealized two-dimensional diagram representing primary vascular architecture in the Arabidopsis inflorescence. Foliage leaves are
represented by squares and flowers by hexagons, numbered according to the ontogenetic helix; symbols represent the approximate level of
the primordium base. Axillary buds (triangles) are associated with cauline leaves 7–9 and with rosette leaves 3–6. After the second flower in
each n + 5 parastichy, traces are derived as branches of vascular sympodia supplying antecedent flowers in the n + 5 parastichy, forming an
open pattern. Accessory bundles (yellow) connect flower traces with adjacent sympodia after seven or more plastochrons. Axillary bud procambial strands (purple) form as branches of either the leaf trace (leaves 3–6) or adjacent sympodia (9) or a combination of the two (7, 8).
The blue line at the base of the illustration represents the solid cylinder of the hypocotyl vasculature. Not to scale.
culature may be elaborated secondarily by the formation of
accessory bundles that provide additional connections between leaf traces and adjacent vascular sympodia (Larson
1980a, 1980b).
Development of vascular architecture and
expression of ATHB8
Despite the progressive elaboration of primary vascular
architecture within rosette and inflorescence stems of Arabidopsis, the developmental steps taking place within the
SAM itself are similar during both vegetative and reproductive phases. Both leaf primordia and floral meristems are
supplied by a single trace that appears to develop acropetally and in continuity with pre-existing vasculature and is
positioned precisely in relation to earlier-formed vascular
bundles and to the placement of newly formed lateral organ
primordia. Based on ATHB8 expression, procambial strand
(or at least preprocambial strand) formation appears to be
coincident with the initial formation of an externally detectable primordium (P1), although detection of primordia from
serial cross sections may have identified only slightly older
primordia (P2 or P3; Kang et al. 2003). During the vegetative stage of development, procambial strands are continuous (based on a combination of anatomical criteria and
ATHB8 expression), with the trace/sympodium procambial
strand corresponding to the n + 8 parastichy. Although this
pattern shifts subtly in the inflorescence (connections correspond to the n + 5 parastichy), the formation of new strands
follows a highly predictable pattern with no indication of a
stochastic component to linkages between strands. The con-
tinuous, acropetal nature of procambial strand formation appears to be general for the dicotyledons, virtually without
exception (Esau 1965a, 1965b) and has been previously reported for Arabidopsis (Vaughan 1955; Busse and Evert
1999).
Although procambial strands within the vegetative and reproductive shoot apical meristems of Arabidopsis appear to
be continuous with antecedent procambial strands, the zone
of ATHB8-GUS expression is initially discontinuous (Kang
et al. 2003). The longitudinally oriented narrow files of cells
below each new primordium express the ATHB8-GUS construct strongly, while ATHB8-GUS activity initially is not
detectable at the basal end where these strands curve to connect with the antecedent parent strand. This stage is ephemeral, as ATHB8-GUS expression becomes established
throughout the length of the leaf trace as the procambial
strand grows in diameter. Such a pattern could indicate that
ATHB8 expression is induced by a basipetally moving signal
and that the discontinuity reflects a moving front that interacts with acropetally moving signals, possibly traveling in
the phloem (reviewed in Lough and Lucas 2006). This idea
is highly speculative, however, as the function of ATHB8 is
still not established; for instance, ATHB8 expression might
simply be a marker of acquisition of xylem cell identity and
only presages the discontinuous nature of xylem differentiation (Kang et al. 2003).
An auxin model that integrates phyllotaxis
and vascular development
The SAM generates regular, predictable patterns of leaves
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and other lateral organs that are generally robust to experimental manipulation (e.g., Reinhardt et al. 2003, 2005;
Smith et al. 2006). Phyllotaxis and the three-dimensional architecture of the vasculature supplying the lateral organs are
highly coordinated in their development. Although the nature of this coordinated development is not yet fully understood, current models point to mechanisms that regulate the
positioning of leaf and floral primordia and of their vascular
supply in an integrated manner. Earlier models of the regulation of phyllotaxis fall into two broad categories: in some
(i), interactions among primordia on the flanks of the shoot
apical meristem are thought to determine the placement of
leaves and flowers, while in others (ii), inductive signals
from older portions of the shoot are thought to play a role
(Larson 1983; Jean 1994; Lyndon 1998; Reinhardt and
Kuhlemeier 2002; Reinhardt et al. 2003). The nature of interactions among primordia is thought to be either biophysical (e.g., Green 1996) or biochemical (e.g., Mitchison 1977;
Schwabe 1984) and to display features of a lateral inhibition
system in which new primordia are placed at the maximum
distance possible from the ‘‘inhibitory’’ antecedent primordia on the flanks of the meristem (Lyndon 1990; Meinhardt
1996). Observations that the placement of new primordia
merely reiterates that of older portions of the shoot and that
developing vascular strands sometimes precede the external
appearance of the primordia that they will supply have led
to suggestions that inductive signals move acropetally
through the vascular system (discussed in Esau 1965a,
1965b; Larson 1983; Lyndon 1990). Current evidence,
however, strongly supports a model in which the phyllotactic pattern is generated within the SAM through biochemical interactions of pre-existing primordia, specifically
through regulation of local variation in auxin concentration.
The auxin model postulates that auxin concentrations act,
not as inhibitors of primordium development, but as active
effectors of a specific developmental sequence of events
(Reinhardt et al. 2003; Reinhardt 2005; Fleming 2004,
2005; Heisler et al. 2005; Smith et al. 2006; Jönsson et al.
2006). The key features of this model (summarized in
Fig. 5) are (i) uniform acropetal movement of auxin in the
surface (L1) layer of the apical meristem from regions outside the SAM, (ii) formation of foci of auxin concentration
in positions that presage the position of primordia through
the polar localization of ATPIN1 proteins, and (iii) redistribution of ATPIN1 polarity upon the outgrowth of primordia
so that polar auxin movement is directed toward the interior
of the meristem, along a narrow file of cells in the position
of the future midvein procambial strand. Support for this
model comes from a number of sources. First, when polar
auxin transport is inhibited by pharmacological treatments,
primordium formation is suppressed (Reinhardt et al. 2000;
Stieger et al. 2002; Benková et al. 2003). Second, as shown
for inhibitor-treated tomato shoot tips or pin1 mutants of
Arabidopsis, suppression of primordium formation can be
reversed by localized auxin treatment (Reinhardt et al.
2000). Third, the auxin efflux carrier protein ATPIN1 accumulates in the L1 layer of the meristem, specifically on the
acropetal side of individual cells, indicating that net movement of auxin is toward the center of the SAM (Benková
et al. 2003; Reinhardt et al. 2003; Heisler et al. 2005).
Fourth, ATPIN1 protein accumulation is strongest in posi-
1667
tions that anticipate primordium formation by one to three
plastochrons (Reinhardt et al. 2003), as is AUXIN RESISTANT 1, a putative auxin influx carrier (Stieger et al. 2002;
Benková et al. 2003). Expression of the reporter construct
DR5-GFP, thought to reflect the endogenous auxin concentration (Benková et al. 2003), also is restricted to the L1
layer of the SAM and expression peaks in incipient primordia (Smith et al. 2006). The phyllotactic pattern of ATPIN1 accumulation is disrupted in the mutants pin1,
pinoid, and monopteros, indicating that auxin signaling
and transport are required for correct PIN1 localization
(Reinhardt et al. 2003). Fifth, ATPIN1 protein is dynamically redistributed during each plastochron: ATPIN1 polarity is first directed toward the center of the presumptive
primordium (I1 in Fig. 5), but with outgrowth, L1 layer
expression decreases and a narrow file of internal cells begins to accumulate ATPIN1 with a basipetal polarity.
(Reinhardt et al. 2003; Heisler et al. 2005; P1 in Fig. 5).
Live imaging of ATPIN1 distribution within the Arabidopsis floral meristem also shows that ATPIN1 concentration
is highest in the I3, I2, and I1 presumptive floral meristem
sites, when the polarity of surface cells adjacent to older,
antecedent primordia is strongly directed toward the center
of the presumptive primordium (Heisler et al. 2005). With
the outgrowth of the primordium, ATPIN1 becomes localized to the basal ends of the internal cells forming a narrow file (Heisler et al. 2005). Thus, the positive induction
of primordium position and vascular strand position by the
localized regulation of auxin concentrations could provide
a single mechanism that regulates both phyllotaxis and vascular architecture, much as hypothesized by Esau (1965a).
The auxin model provides a mechanism for the formation
of leaf trace procambial strands in a pattern that is coordinated with phyllotaxis, but almost all aspects of how the initial pattern of ATPIN1 distribution is translated into the
complex three-dimensional vascular architecture of the shoot
are unknown. In many ways, the localization of ATPIN1
protein to an internal strand of cells during the early plastochrons of primordium development (Reinhardt et al. 2003;
Heisler et al. 2005) is comparable with the generation of
the two-dimensional, yet complex, pattern of leaf veins. In
developing leaves, PIN1 is expressed first in the protoderm
(derived from the L1 layer) and PIN1-GFP protein is localized subcellularly to the acropetal side of protodermal cells,
producing a convergence point at the apex (Scarpella et al.
2006); thus, the pattern observed for the SAM is preserved
during early stages of leaf development. Internal cells adjacent to the apical convergence point accumulate PIN1-GFP
at the basal side of the cells, and the zone of expressing
cells extends towards the base of the leaf, forming the midvein prepattern (Scarpella et al. 2006). The looped secondary veins are generated similarly, starting with a
convergence point at the leaf margin and with a series of
cells expressing PIN1-GFP extending toward the midvein.
These cells accumulate PIN1-GFP on the side toward the
midvein, suggesting that auxin moves along the incipient
vein from a source at the margin to the sink represented by
the earlier-formed strand (Scarpella et al. 2006).
Strands of preprocambial tissue are polar in their development and extend unidirectionally from pre-existing strands;
if strand extension is arrested, a ‘‘freely ending veinlet’’ is
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2006 NRC Canada
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Can. J. Bot. Vol. 84, 2006
Fig. 5. Idealized two-dimensional diagram representing the spatial pattern of polar auxin flow (based on localization of the ATPIN1 protein:
Reinhardt et al. 2003; Heisler et al. 2005) and of ATHB8 expression (based on promoter-GUS expression: Kang et al. 2003) in vegetative
and inflorescence SAMs of Arabidopsis. Arrows, coinciding with localization of ATPIN1, indicate net movement of auxin toward the centers of incipient primordia (I1, I2) and toward internal tissue during early primordium outgrowth (P1, P2). An isolated file of ATHB8-GUSexpressing cells (blue) is present at the P1 and later stages below the base of the primordium, although a connecting strand of anatomically
defined procambium (pink) is consistently present, connecting it to the antecedent procambial strand associated with a leaf that is eight
plastochrons older (vegetative SAM).
formed. During the development of most of the secondary
and higher-order venation, however, strand extension rapidly
connects with an adjacent strand, thus forming a continuous
link between pre-existing strands (Scarpella et al. 2004,
2006). The prepatterns represented by PIN1-GFP, the auxin
reporter DR5-GUS, the gene trap marker ET1335-GUS, or
ATHB8-GUS all appear when the leaf (or field of tissue for
higher-order veins) consists of relatively few cells and is extended by intercalary growth as the leaf enlarges (Mattsson
et al. 2003; Kang and Dengler 2004; Scarpella et al. 2004,
2006); thus, the stage of discontinuity and unidirectional
growth is ephemeral (except for the freely ending veinlets).
The cytological features of cells expressing these markers
are indistinguishable from those of cells of the ground tissue
in which this preprocambial pattern arises; only later do the
distinctive elongate shape and dense cytoplasm of anatomically defined procambial cells emerge (Mattsson et al.
2003; Kang and Dengler 2004; Scarpella et al. 2004, 2006).
Thus, elements of pattern formation are shared by development of both two-dimensional leaf vein patterns and threedimensional shoot vascular pattern: (i) unidirectional
elaboration of the system that may reflect auxin transport
from localized sources to sinks within the tissue, (ii) formation of major elements of the system, such as leaf primary
and secondary veins or the n + 8 sympodial strands of the
stem followed by formation of minor pattern elements, such
as the higher order venation or the n + 5 sympodial strands,
and (iii) discontinuities in the accumulation pattern of certain
proteins, such as that observed for PIN1 expression in an in-
cipient leaf primordium (Reinhardt et al. 2003; Heisler et al.
2005) or in the expression of ATHB8 within leaf traces
(Kang et al. 2003). An important distinction between the
two is that while leaf vein pattern development points to a
highly flexible self-organizing patterning mechanism (Scarpella et al. 2006), shoot vascular architecture appears to be
highly predictable, with almost no stochastic element to the
formation of connections between strands (Kang et al. 2003).
Future prospects
Plants are increasingly regarded as supracellular organisms in which long-distance transport of, not only water and
dissolved nutrients, but also of macromolecules and other
signaling substances depends on the vascular system (Lough
and Lucas 2006). Knowledge of the three-dimensional architecture of the vascular system, and particularly how it corresponds to leaf position on the shoot, is essential for
understanding how photosynthate moves through the phloem
from specific source to specific sink leaves or how chemical
defense signals might move from herbivore-damaged leaves
to particular newly expanding ones (e.g., Larson 1977;
Marshall 1996; Orians and Jones 2001). For instance, in
poplar, when 14C label was supplied to a photosynthesizing
source leaf, it was possible to predict where the relative
percentages of the labeled photosynthates would appear
based on knowledge of the connections of central and lateral leaf traces with adjacent vascular sympodia and of the
transitions in phyllotaxis appearing during shoot ontogeny
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2006 NRC Canada
Dengler
(Larson 1977). Analyses of phloem sap and use of grafting
between stocks and scions of different genotype have demonstrated that numerous macromolecules function in longdistance communication and use phloem tissue as a conduit
(reviewed by Lough and Lucas 2006). One example of
these is the FLOWERING LOCUS T protein, a component
of a phloem-mobile florigenic signal. Induction of gene expression in a source leaf by heat shock results in accumulation of FLOWERING LOCUS T mRNA in both the
source leaf and the SAM, indicating that the mRNA (or
perhaps the protein) moves along the vascular sympodium(a) connecting the source leaf and the primordia closest to the SAM (Huang et al. 2005). Although many
environmental and developmental stimuli may not be localized, so that signaling moves through the entire shoot vasculature and affects leaves of all parastichies equally, many
triggers will be specific to regions of the shoot or root system, and vascular architecture will contribute to determining which targets will be reached by those signals.
Knowledge of shoot primary vascular architecture of Arabidopsis, specifically, might form the basis for better understanding aspects of the developmental biology of this model
organism. The information described herein is especially
useful for the interpretation of mutations that affect the vascular system, for instance the supernumerary vascular bundles that appear in mutants such as REVOLUTA (Zhong et
al. 1999) or the effects of mutants in other HD-ZIP family
genes on shoot vascular pattern as well as ground sclerenchyma (Prigge et al. 2005). Expression patterns of genes
such as ATHB8 or DR5 that are restricted to developing
procambial strands might be used in mutant screens to
identify genes that function in the construction of this
complex three-dimensional pattern. Although the analysis
presented here was based on laborious reconstruction from
serial cross sections (Kang et al. 2003), analysis of cleared
whole shoots of plants carrying these reporter constructs or
use of confocal microscopy and other imaging systems
would allow identification of mutants. Most importantly,
knowledge of the primary vascular system of Arabidopsis
and how it remains coordinated with changes in phyllotaxis
and organ identity through juvenile, vegetative adult, and
reproductive phases will contribute to understanding the
genetic framework that underlies shoot development.
In summary, developmental biologists have made dramatic headway in providing evidence from gene reporter
studies, experimental manipulations, and modeling that
strongly support the role of the PIN proteins in the regulation of localized auxin concentrations, leading to the patterned initiation of leaf primordia in the correct phyllotactic
sequence on the flanks of the SAM. Tantalizingly for the
topic at hand, the subcellular localization of PIN1 proteins
in Arabidopsis indicates that auxin flows from the center of
the primordium site inwards along a narrow path, presaging
the location of the leaf midvein and its connecting leaf
trace. Thus far, imaging techniques have been limited to
surface layers, so it has not been possible to ‘‘connect the
dots’’ and relate this midvein prepattern with the predicted
connection of the leaf trace with the vascular sympodium
corresponding to the n + 8 parastichy. Detailed analysis of
the development of leaf vein pattern indicates that localized
concentrations of auxin also initiate the expression of a pro-
1669
cambial prepattern that connects a source of auxin with tissues acting as a sink and that reiterations of the process
create a complex hierarchical pattern (Scarpella et al.
2006). Although such concentrations only have been shown
to occur in the L1 layer of the SAM and the protoderm of
developing leaves, a similar process is likely to occur within
internal ground tissues and would be integral to the generation of the three-dimensional vascular pattern of shoots and
to its secondary modification during development.
Acknowledgments
I thank Thomas Berleth, Julie Kang, Bill Remphrey, and
two anonymous reviewers for helpful comments on the
manuscript, Janice Wong for illustrations, and the Natural
Sciences and Engineering Research Council of Canada for
research support.
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