Phyllotaxis — a new chapter in an old tale about beauty and
magic numbers
Didier Reinhardt
Phyllotaxis, the regular arrangement of leaves and flowers
around the stem, is one of the most fascinating patterning
phenomena in biology. Numerous theoretical models, that are
based on biochemical, biophysical and other principles, have
been proposed to explain the development of the patterns.
Recently, auxin has been identified as the inducer of organ
formation. An emerging model for phyllotaxis states that polar
auxin transport in the plant apex generates local peaks in auxin
concentration that determine the site of organ formation and
thereby the different phyllotactic patterns found in nature. The
PIN proteins play a primary role in auxin transport. These
proteins are localized in a polar fashion, reflecting the
directionality of polar auxin transport. Recent evidence shows
that most aspects of phyllotaxis can be explained by the
expression pattern and the dynamic subcellular localization of
PIN1.
Addresses
University of Fribourg, Department of Biology, Plant Biology Unit,
Rte Albert Gockel 3, CH-1700 Fribourg, Switzerland
Corresponding author: Reinhardt, Didier (didier.reinhardt@unifr.ch)
Current Opinion in Plant Biology 2005, 8:487–493
This review comes from a themed issue on
Cell signalling and gene regulation
Edited by George Coupland and Salome Prat Monguio
Available online 28th July 2005
1369-5266/$ – see front matter
# 2005 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2005.07.012
Introduction
The leaves, flowers and floral organs of plants are arranged
in regular patterns, a phenomenon referred to as phyllotaxis
[1]. The prevalent phyllotactic patterns found in
nature are distichous (alternate), decussate (opposite) and
spiral. Spiral phyllotaxis is the most widespread pattern
and is found in mosses, ferns, gymnosperms and angios-
perms.
Spiral phyllotaxis has long been of interest to theoreticians
because of its peculiarity in following mathematical
rules characterized by the Fibonacci numbers [1,2]. By
contrast, experimental approaches aimed at revealing the
regulation of phyllotaxis have been hampered by the
delicacy and the minute size of the meristem in which
the organs are formed and their position (and hence the
resulting phyllotactic pattern) determined [1]. Moreover,
genetic approaches to study phyllotaxis have frequently
been complicated by the pleiotropic phenotypes of many
phyllotactic mutants [3].
During the past few years, however, thanks to the molecular-genetic
tools developed in Arabidopsis and to
improved experimental techniques, phyllotaxis has
become more amenable to direct experimentation. Thus,
it became possible to test directly biophysical and biochemical
models of phyllotaxis by direct local application
of growth regulators to the meristem [4] and by laser
ablation of subdomains of the meristem [5]. Biophysical
models have received little experimental support,
whereas recent evidence supports a biochemical mechanism
for phyllotaxis with auxin at its centre.
Leaves ‘repel’ each other
Leaves tend to be formed at a certain minimal distance
from each other. This is obvious in distichous phyllotaxis,
in which leaves are formed in two opposite vertical rows,
as for example in maize. In this case, the divergence
angle, that is the angle between successive leaves, is 1808.
In decussate phyllotaxis, leaves are formed in pairs with
opposite position and subsequent pairs diverge by 908.
Thus, in distichous and decussate phyllotaxis, leaves are
formed at maximal distance from each other.
How could the spacing be explained in the case of spiral
phyllotaxis in which successive leaves diverge by 137.58?
One possibility is that leaf position is controlled by the
two youngest primordia in an asymmetric fashion, with
the youngest primordium (P1) having a stronger repelling
effect than the second youngest (P2), thus forcing the new
primordium (I1) to be formed closer to P2 than to P1
(Figure 1; [6]. Indeed, the two youngest primordia (P1 and
P2) are sufficient to determine the approximate position
of I1, and therefore the direction of the phyllotactic spiral
(clockwise or counter clockwise) [7
]. Nevertheless, older
primordia in the vicinity of I1 and P1 are important for
their lateral delimitation [7
], thereby defining their exact
final position. Although, the existence of a ‘repelling
mechanism’ of some sort was first documented 70 years
ago [8], the nature of the mechanism involved remained
elusive until recently.
Auxin comes into the play
Several mutants that have defects in auxin production,
transport, or perception exhibit defects in organ initiation,
position, number, and delimitation as part of their pleiotropic
phenotype [9–15]. This indicated an important role
for auxin in organ formation and phyllotaxis. It has been
www.sciencedirect.com Current Opinion in Plant Biology 2005, 8:487–493
shown that the natural auxin indole-3-acetic acid (IAA)
acts as an inducer of organogenesis and influences organ
position [4]. Moreover, the expression pattern of an auxinresponsive
reporter gene showed high levels of auxin
activity at the site of leaf and flower formation [16].
Together, this evidence suggests that auxin might be
more than just a permissive factor that is required to
promote growth (like a vitamin or an essential component
of the cell cycle), but rather acts as an instructive signal: a
morphogen [17].
Is auxin the phyllotactic morphogen?
The simplest mechanism to account for a ‘repelling’
influence of pre-existing primordia on new primordia
would be the release of an inhibitor of leaf formation
[6]. However, experimental support for such an inhibitory
substance is missing. The observation that auxin influences
leaf formation and positioning has opened exciting
new possibilities for models of phyllotaxis. Could the preexisting
primordia determine the position of new primordia
by influencing auxin distribution in the meristem? If
primordia accumulate auxin from their vicinity, they
could generate peaks in auxin concentration and, at the
same time, lead to auxin depletion in their vicinity. Such a
mechanism would be attractive because it explains the
different aspects of phyllotaxis (i.e. organ positioning,
initiation and lateral delimitation) through the activity
of one signal, auxin. Furthermore, such a model would be
consistent with the pleiotropic phenotypes observed in
auxin-related mutants such as pinformed1 ( pin1), pinoid,
and monopteros.
An instructive function implies that differences in auxin
concentration are perceived and interpreted by the meristem
cells that are deciding which identity to acquire (i.e.
organ or non-organ). In a tissue as small as the meristem,
the size of which ranges between 50 and 150 mm, however,
a small molecule such as IAA (Mr = 175.2) would be
expected to diffuse rapidly, thus dissipating concentration
differences within minutes. Therefore, the generation
and maintenance of auxin concentration gradients in
the meristem would require active directional transport. A
central component of the active and selective auxin
transport system is represented by the PIN protein
family, which is involved in auxin efflux from cells [18].
An auxin-based model of phyllotaxis
Polar auxin transport, the directional transport of auxin
within a tissue, is mediated by cellular influx and efflux
carriers that frequently exhibit an asymmetric subcellular
localization [10,19–22]. Auxin can also be transported in
the phloem from the sites of synthesis in young organs to
sink tissues such as the root [19]. Auxin transport via
phloem cannot occur in the meristem, however, because
functional vascular strands are not present in this tissue.
The shoot meristem of Arabidopsis expresses AUXIN
RESISTANT1 (AUX1), the founding member of the
family of putative auxin influx carriers (AUX/LAX family)
[23], as well as PIN1, a member of the efflux regulator
family (PIN family) [18]. AUX1 is expressed in the
epidermal L1 layer of the meristem, indicating that cells
within this layer accumulate auxin [24]. PIN1 is
expressed in the same cells, with an asymmetrical localization
on the upper end of the cells (pointing towards
the meristem centre), suggesting that auxin is transported
upwards into the meristem through the L1 layer ([24];
Figure 2).
Importantly, PIN1 expression is also induced very early in
organogenesis, when its subcellular localization indicates
that auxin accumulates in the centre of the young organs
([24]; Figure 3). Taken together, these observations support
the following model (Figure 4): first, auxin is delivered
uniformly throughout the meristem with no
preferred position around the periphery (Figure 2). Second,
auxin accumulates in primordia and is depleted in
their vicinity (Figure 3). Third, by default, auxin accumulates
at a certain minimal distance from the pre-existing
primordia (which is beyond the ‘reach’ of the
primordia) (Figure 4a). At this point, auxin induces
PIN1 expression and early founder cell identity. This
initiates the active accumulation of auxin, resulting in a
sharp auxin peak and leading to delimitation of the future
organ and auxin depletion from the surrounding cells
(Figure 4b). Finally, a new primordium grows out at
the site of the auxin peak (Figure 4c).
488 Cell signalling and gene regulation
Figure 1
I1
MP1
P2
Current Opinion in Plant Biology
Schematic representation of an apex with spiral phyllotaxis. P1 and
P2 are the youngest primordia, the yellow area represents the
meristem (M) with the site of incipient leaf formation in red (I1). P1
and P2 (green) diverge by 137.58. I1 is positioned in an asymmetric
way closer to P2 than to P1.
Current Opinion in Plant Biology 2005, 8:487–493 www.sciencedirect.com
This model explains the reiterative nature of phyllotaxis
and is consistent with the results of microsurgical and
laser ablation studies. Remarkably, ablations of the meristem
centre do not affect phyllotaxis [5,25], whereas
isolation or ablation of young primordia leads to a shift
in position of the subsequent primordia [7
,8]. These
observations are compatible with a function of primordia
as auxin sinks.
A feature of this model is the conceptual separation of
polar auxin transport into an acropetal (i.e. upward) component
that is responsible for the delivery of auxin to the
meristem (with no phyllotactic information), and a component
that mediates the redistribution of auxin in the
organogenic periphery (and represents the phyllotactic
component of auxin transport). This aspect of the model
is in agreement with the observation that inhibition of
auxin transport can lead to seemingly contradictory consequences:
depending on the stage of plant development
and on the experimental conditions, it leads either to the
production of bigger and fused organs or to a complete
block in organ formation [4,9]. I suggest that in the latter
case, the patterning defect is hidden because of the lack
of auxin in the meristem, whereas in the former, enough
auxin is supplied to the meristem to reveal the patterning
defect. The fact that pin1 mutants are capable of organ
formation under certain conditions suggests either that
redundant functions of related auxin efflux carriers are
active at these stages or that the sources of auxin are close
enough to the meristem to allow auxin to reach the
meristem by diffusive transport. In this context, it is
interesting to note that the cessation of organogenesis
in pin1 coincides with the onset of bolting, whereby the
shoot apical meristem becomes progressively more distant
from the rosette leaves.
Where does auxin come from?
In general, young tissues such as growing leaves and
developing flowers produce auxin [26,27], but we do
not know at which stage of primordium development
auxin biosynthesis commences. The lack of organ formation
in pin1 mutants and in apices that have been treated
with auxin transport inhibitors suggests that auxin is not
produced in the meristem itself [4]. However, small apical
explants that retain only the meristem and one primordium
with a little bit of submeristematic tissues are
capable of organ formation without a delay, suggesting
that the sources of auxin are close to the meristem [7
].
Similarly, when meristems of pin-shaped apices were
relieved from transport inhibition, they resumed leaf
formation despite the absence of pre-existing leaves
[4]. This suggests that stem tissues are capable of sufficient
auxin production to promote organ formation. However,
the relative contributions of the different tissues in
the apex (i.e. primordia, stem and meristem) to auxin
biosynthesis remain largely unknown.
What is upstream of PIN1?
A central feature of our phyllotactic model is the regulation
of PIN1 localization. How is the polar localization of
the efflux carriers controlled? Although little is known
about the mechanism of initial polarization, we have
started to understand how PIN1 localization is regulated
in the polarized cell. PIN1 is continuously endocytosed to
endosomal compartments, and recycled back to the plasmalemma,
thus providing a dynamic cellular mechanism
that enables rapid changes in PIN1 localization [28].
Hence, it appears that the site of integration of PIN1containing
vesicles into the plasmalemma determines the
steady-state subcellular localization. The recycling of
PIN1 requires the vesicular trafficking system as a workhorse;
but how does the cell know where to deliver its
cargo? An important determinant of PIN1 localization is
the protein kinase PINOID (PID) [29
]. Although PID
might not be involved in the polarization of the cells per se,
it influences the way in which cells interpret this information
and allocate the PIN1 protein. PID decides at
which end of the polarized cell PIN1 will accumulate.
Consequently, PID can act as a switch that funnels auxin
in one direction or the other. This effect has been
observed in several cell types in the root and the shoot
apex, including the meristem L1 layer [29
]. A probable
explanation for the similarity of the pin1 and the pid
phenotypes is that, in pid mutants, auxin transport in
L1 goes in the wrong direction, away from the meristem.
Is PID also involved in the patterning aspect of phylloPhyllotaxis
Reinhardt 489
Figure 2
Current Opinion in Plant Biology
P2
M
P1
Auxin transport in the epidermal L1 layer of the shoot meristem.
L1 cells express the presumptive auxin influx carrier AUX1, leading
to the accumulation of auxin in L1 (green arrows). PIN1 is also
expressed in the L1 layer, where it is localized to the upper side of
the cells (light blue). This results in the acropetal transport of auxin
towards the meristem centre (blue arrows). Inset: the depicted
area in the context of the apex.
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taxis? Although pid mutants exhibit patterning defects
during embryogenesis and flower formation, they appear
more normal than pin1 during vegetative development
[11], and they retain at least part of their patterning
capacity in the inflorescence meristem [24]. Hence, not
all aspects of PIN1 subcellular localization appear to be
regulated by PID. Redundant functions of PID-related
proteins might be involved in regulating PIN1 localization
in these cases.
Does auxin influence PIN1 expression and localization?
Auxin triggers the differentiation and patterning of vascular
strands [30]. These contain the PIN1-expressing
xylem parenchyma cells, the site of polar auxin transport
[10]. Thus, besides acting downstream of PIN1 as a
transport substrate, auxin can also function upstream of
PIN1 by determining the direction and capacity of its own
transport routes. This dual role of auxin is also a feature of
phyllotaxis, in which PIN1 expression is induced at the
site of organ formation [24,31] or by exogenous auxin [24].
Moreover, the subcellular localization of PIN1 also
responds to phyllotactic information, providing a feedback
mechanism for the reiterative progression of phyllotaxis
([24]; Figures 3 and 4). It remains to be seen,
however, whether PIN1 localization is influenced directly
by auxin, or whether a secondary signal released from
founder cells and young primordia can relay the phyllotactic
information provided by auxin gradients.
490 Cell signalling and gene regulation
Figure 3
P4
P1
P3
P2
P5
Current Opinion in Plant Biology
Auxin accumulation in young primordia. PIN1 is induced in young primordia. It becomes localized to the side of the cells that points to the centre
of the primordium (light blue). This results in the accumulation of auxin in the primordium and its withdrawal from the surrounding cells (blue
arrows). The resulting auxin gradient (red) confers positional information to the cells allowing them to establish organ and boundary identity.
Inset: Location of the P1 position in the context of the apex.
Current Opinion in Plant Biology 2005, 8:487–493 www.sciencedirect.com
Downstream events in organ formation
Little is known about auxin perception and signal transduction
in the meristem. Although a candidate for an
auxin receptor has been characterized [32], its role in
auxin perception in the meristem is not known. Recent
evidence shows a prominent role for the F-box protein
TRANSPORT INHIBITOR RESPONSE1 (TIR1), a
subunit of the SKP1 CULLIN F-BOX/RING-H2
(SCF) complex, in auxin perception [33
,34
]. In the
absence of auxin, AUX/IAA proteins (i.e. proteins
expressed by genes that are induced by auxin and IAA)
prevent an auxin response by binding, and thereby inhibiting,
auxin response factors (ARFs), which are transcriptional
regulators of downstream auxin responses [35]. In
the presence of auxin, AUX/IAA proteins become ubiquitinated
by the SCFTIR1
complex and subsequently
degraded by the 26S proteasome [36], thus leading to the
release of the ARFs and the activation of the auxin
response. TIR1, a component of the ubiquitin ligase
complex SCFTIR1
, directly binds auxin and therefore acts
as an auxin receptor [33
,34
]. Mutations in the ARF
gene MONOPTEROS (MP) lead to a block in organogenesis
similar to that observed in the pin1 mutant [14]; in
contrast to pin1, however, the meristem of mp mutants
does not respond to exogenous auxin [24]. These results
document the role of MP in the downstream signal
transduction of the auxin signal in organ formation.
Many genes in the meristem are expressed in a phyllotactic
pattern [3] (i.e. their expression responds to the
phyllotactic patterning machinery). At the site of incipient
organ formation, members of the KNOX
(KNOTTED-like homeobox) gene family, which confer
meristem identity, are downregulated, reflecting the
acquisition of founder cell identity [37]. Other genes play
a crucial role in the elaboration of the organs by defining
organ boundaries (NO APICAL MERISTEM and CUPSHAPED
COTYLEDON) [38,39], organ identity (LEAFY)
[40], and patterning of the developing organs (PHANTASTICA
and PHABULOSA) [41,42]. In the pin1 mutant,
genes that are normally expressed in a phyllotactic pattern
loose this pattern [31], indicating their position
downstream of auxin. However, the transport regulators
PIN1 and PID themselves loose their phyllotactic expression
patterns in the pin1 mutant, demonstrating their
dependence on patterning by auxin. This apparent paradox
is due to the fact that phyllotaxis is not regulated by a
pathway that is organised into a linear hierarchy but by a
mechanism that involves feedback regulation (see also
previous section). Therefore, downstream genes that are
expressed in developing organs might modulate their
auxin sink activity, thereby influencing auxin distribution
in the meristem and, as a consequence, the positioning
and development of future primordia. In this way, genes
that are downstream of auxin (considering the developing
primordium P1) could, indirectly, function upstream of
auxin relative to the position of the next primordium (I1).
For further discussion of founder cell identity and downstream
regulatory mechanisms in primordium development,
the reader is referred to two recent reviews [43,44].
Factors independent of auxin
Besides the range, capacity and rate of auxin transport,
other parameters such as meristem size, growth rate and
Phyllotaxis Reinhardt 491
Figure 4
Current Opinion in Plant Biology
(a) (b) (c)
P3
P2
P1
I1
P1
P2
P2
P3
P1
Progression of organ positioning and outgrowth during the phyllotactic cycle. (a) As a result of the sink function of P1 and P2, auxin that is delivered
to the meristem by acropetal auxin transport becomes diverted into the primordia (arrows). As a result, auxin (red) can accumulate only slowly
at a defined minimal distance from P1 and P2, which corresponds to the site of incipient organ formation (I1). (b) At a certain threshold level of
auxin, PIN1 becomes induced and begins to actively accumulate auxin at I1. At the same time, the sink activity of P1 and P2 decreases. (c) Auxin
has been focused to a sharp peak at I1, leading to the outgrowth of a new organ. Thus, the apex has progressed by one plastochron compared to
that shown in (a) (note the change in the nomenclature of primordia). Arrows represent the direction of polar auxin transport; auxin distribution is
represented in red. For clarity, only auxin at I1 is depicted.
www.sciencedirect.com Current Opinion in Plant Biology 2005, 8:487–493
apical–basal extension growth can be expected to influence
phyllotaxis because they indirectly influence auxin
transport and the size of the field in which auxin operates.
Indeed, changes in cytokinin homeostasis that affect
meristem size in maize can lead to a change from distichous
to decussate phyllotaxis [45
]. It is conceivable
that merely increasing meristem size leads to this dramatic
transition, simply by creating space for two leaves to
be formed at a time instead of one. Likewise, in the
ultrapetala mutation of Arabidopsis, an increase in organ
number is associated with an increase in meristem size
[46].
Nevertheless, increased organ number and changes in
phyllotactic patterning can also occur in the absence of
changes in meristem size: as observed, for example, in the
mutants perianthia and bellringer [47,48]. The homeobox
protein BELLRINGER and members of the KNOX
family of homeobox transcription factors are involved
in a regulatory network that controls the biosynthesis
of, and response to, the phytohormones gibberellin and
cytokinin in the meristem [49]. Thus, cytokinin, gibberellin,
and perhaps other signals can influence phyllotaxis
independently of auxin by modulating tissue growth and
cell differentiation in the apex.
Conclusions
At the centre of phyllotaxis is auxin, together with PIN1
and PID, which regulate its transport, and MP, which is
involved in signal transduction. However, additional
upstream and downstream components remain to be
identified. Many of the biochemical and molecular details
of auxin biosynthesis, transport and perception are still
elusive. In particular, the feedback loop that is a central
component of the reiterative phyllotactic mechanism
remains to be characterized.
Computer modelling has traditionally been employed to
develop and test mechanisms of phyllotaxis [2,50–53].
Because of the lack of information on the molecular/
cellular basis of phyllotaxis, however, most of these
models remained largely abstract. Some of them also
failed to express characteristic features such as the robustness
and the self-correcting properties of phyllotaxis.
With the detailed information from experimental work
that is now available, we can build models that are closer
to reality. Starting from simulations on the level of small
populations of cells [54], it will be possible to generate
integrated models that exhibit the known features of
phyllotaxis. Such models will help to design future
experiments and will direct our attention to crucial questions
that remain to be answered. Furthermore, such
models might provide hints as to how developmental
phenomena, such as the transition from decussate to
spiral phyllotaxis in dicotyledonous plants, could be
regulated. Ultimately, the combination of experimental
and theoretical approaches promises to reveal the origin
of phyllotaxis.
Acknowledgements
I thank Jiri Friml, Cris Kuhlemeier, Przemek Prusinkiewicz and Sam
Zeeman for critical reading of the manuscript. This work was supported
by a grant from the Swiss National Science Foundation
(SNF 31-55540.98).
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