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Pattern formation during early floral development
Prasad Vaddepalli, Sebastian Scholz and Kay Schneitz
Flowers are central to sexual reproduction in plants. The
study of floral development proved tremendously successful
in obtaining key insight into processes, such as fate
determination, pattern formation, and growth regulation.
Recent advances relate to the complex mechanisms
underlying the crosstalk between phytohormone signaling, cell
and tissue mechanics, and regulatory gene networks that
positions floral buds at the apex and directs floral
specification, initiation and outgrowth. Furthermore, progress
has been made in elucidating the intercellular communication
and temporal coordination necessary to organize the behavior
of the various functional subdomains within the young flower.
Addresses
Entwicklungsbiologie der Pflanzen, Wissenschaftszentrum
Weihenstephan, Technische Universitat Munchen, Emil-Ramann-Str.
4, 85354 Freising, Germany
Corresponding author: Schneitz, Kay (kay.schneitz@tum.de)

Current Opinion in Genetics & Development 2015, 32:1623

This review comes from a themed issue on Developmental
mechanisms, patterning and organogenesis
Edited by Deborah J Andrew and Deborah Yelon
For a complete overview see the Issue and the Editorial
Available online 16th February 2015
http://dx.doi.org/10.1016/j.gde.2015.01.001
0959-437X/# 2015 Elsevier Ltd. All rights reserved.

Introduction
In contrast to animals, most organogenesis in plants occurs
post-embryonically. Following fertilization the embryo
develops into an inconspicuous seedling that carries two
growth centers at its opposite ends: the shoot and root
meristems. Upon seedling germination, above-ground
lateral organs, such as leaves or flowers, ultimately derive
from the shoot apical meristem (SAM).
During the reproductive phase of the life cycle, the SAM
produces floral primordia that quickly develop into floral
meristems (FMs) that, in turn, originate floral organs, such
as sepals or carpels (Figure 1a). The SAM and FM are
characterized by several distinct groups of cells (Figure
1b). In the central zone (CZ), a small cluster of rarely
dividing stem cells remains in an undifferentiated state
throughout the life of the SAM. Progeny of these cells will
end up in the flanking peripheral zone (PZ) where cell
division rates are higher and lateral organ
Current Opinion in Genetics & Development 2015, 32:1623

formation is initiated at certain positions. Underneath the

stem cells, the organizing center (OC) within the rib
meristem provides a niche required for stem cell induction
and maintenance. The SAM and FM are also organized into
clonally distinct layers [1] that are main-tained by oriented
cell divisions. Cells in the L1 (epider-mal layer) and the L2
(uppermost sub-epidermal layer) divide strictly anticlinally
(perpendicular to the surface of the meristem). The L3
comprises the more interior cells that divide in an
apparently irregular fashion.
The phytohormone auxin and the cell wall represent
essential factors in plant development. Auxin signaling
mechanisms are complex and differ depending on wheth-er
auxin perception occurs inside the cell or in the extracellular matrix [2]. Binding of auxin to the nuclear TIR1/
AFB F-box protein auxin receptor results in the degradation of AUX/IAA transcriptional repressors (Table 1) and
the concomitant de-repression of their binding partners,
transcriptional regulators of the AUXIN-RESPONSE
FACTOR (ARF) family [3]. Extracellular auxin percep-tion
involves a complex of AUXIN-BINDING PRO-TEIN1
(ABP1) and the receptor-like kinase TMK1, which
regulates further cellular processes through the
activation of plasma membrane-associated GTPases, such
as ROP6 [4 ].
The semi-rigid cell wall cross-links plant cells and is a
crucial determinant of the direction and rate of growth. Cell
growth is driven by a combination of isotropic internal
turgor pressure, cell wall loosening, and subse-quent
incorporation of new wall material [5]. The direc-tion of
cell elongation is dictated by load-bearing cellulose
microfibrils in the cell wall whose orientation, in turn,
depends on the orientation of the cortical micro-tubules
(CMTs) [6]. Thus, direction of growth is influ-enced by cell
wall anisotropy in growing cells.
This brief review focuses on some prominent insights into
the mechanisms underlying the coordination of pattern
formation, growth, and hormone signaling during early
floral development that were obtained in the last two years.
Different perspectives on floral development can be
obtained from several other excellent reviews [710].

Positioning floral primordia

In phyllotaxis, lateral organs, such as leaves or flowers,
arise in a typical stereotypic pattern at the periphery of the
SAM. Organ formation is triggered by local auxin maxima
in the L1 of the PZ [1113]. Auxin is produced throughout
the meristem and robust spiral phyllotaxis depends on
auxin biosynthesis in the center of the SAM
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Early floral development Vaddepalli, Scholz and Schneitz

17

Figure 1

(a)

(b)

(c)

P3

auxin

L1
P5

CZ

P6

PZ
P1

L1

L2 L3
PZ

se

se

MP

DELLA

GA
AP1
Fate

P2

P4

se
P7

ELA1

MAB4

SPL

PIN1

LFY
MP

Initiation

auxin
auxin

ANT
AIL6

Current Opinion in Genetics & Development

An overview of early flower development. (a) Scanning electron micrograph providing a top view onto the shoot apical meristem in Arabidopsis
thaliana. Floral primordia at different stages are indicated with the youngest primordium denoted P1. A sepal primordium (se) in P7 is indicated. Scale
bar: 10 mm. (b) Confocal micrograph depicting a vertical mid-optical section through a stage 3 floral meristem. At this stage the meristem is flanked by
sepal primordia (se). The approximate arrangement of the central zone (CZ) and the peripheral zone (PZ) is indicated. Scale bar: 10 mm.
(c) Schematic summarizing the interplay between auxin, MP, LFY, and gibberellin during early floral development. Processes/factors involved in
polar auxin transport are marked in blue. Adapted from [27 ,28 ,35,36 ].

[14 ]. Redistribution of auxin to sites of organ initiation

requires active polar auxin transport depending on the PINFORMED (PIN) family of auxin exporters [15]. Plasma
membrane-bound PIN members are polarly lo-calized
within the cell, with the site of PIN accumulation predicting
the direction of auxin flow. PINs are activated through
phosphorylation by plasma membrane-associated AGC
VIII protein kinases, including D6 PROTEIN KINASE
(D6PK) and PINOID (PID) [16 ].
In the prevalent notion, discrete auxin maxima in the PZ
are, in part, the result of a growth-promoting positive
feedback loop between tissue mechanics and PIN1-mediated polar auxin transport in the L1 where PIN1 orientation, and thus auxin flux, converges toward higher auxin
concentration (up-the-gradient) [1720]. In line with this
notion, PIN1 expression in the L1 is necessary and sufficient for correct positioning of floral primordia [21 ]. Apart
from positioning floral primordia, auxin affects the timing
of organ initiation through influencing signal transduction
mediated by the phytohormone cytokinin [22 ].

Early flower development

Once a site of flower initiation has been determined, a
group of floral organ founder cells develops into a floral
primordium. A central question relates to how primordi-um
initiation, specification and proliferative growth are
coordinated during early floral development.
To initiate a new floral primordium, and thus a new growth
axis, the local presence of high auxin at the flank of the
shoot apex has to overcome the anisotropic growth that
controls the main growth direction of the stem [23].
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The microtubule-severing protein katanin (KTN1) contributes to the formation of anisotropic CMTs [24]. Recent
evidence indicates that, at low levels of auxin, the extracellular auxin receptor ABP1, the GTPase ROP6 and its
effector RIC1 maintain anisotropic CMTs through a regulation of KTN1 function [25 ]. During early primordium
development, however, high local auxin somehow overrules this mechanism and initiates isotropic growth. Computer modeling suggested that a combination of two auxinmediated effects, a limited reduction in cell wall stiffness
and an increase in growth isotropy, was sufficient to
promote organogenesis in a robust manner [25 ].
Analysis of downstream responses of auxin signaling
mediated by the auxin response transcription factor (TF)
MONOPTEROS (MP)/ARF5 has led to substantial insight
into the coordination of floral primordium initia-tion,
specification and proliferative growth. MP activates a set of
genes, which exhibit separate and shared func-tions during
early floral development.
A dynamic reorganization of subcellular PIN1 localization
represents an early sign of floral primordia initiation. A few
L1 cells at the center of the developing primordium orient
PIN1 toward the interior of the primordium [11,26]. This
so-called basipetal reorientation ultimately results in the
generation of an auxin sink and accu-mulation of auxin in
the interior of the outgrowing pri-mordium. It is of central
importance for the further development of the floral
primordium [27 ].
Recent work revealed that MP activates the expression of
members of the NON-PHOTOTROPIC HYPOCOTYL 3
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18 Developmental mechanisms, patterning and organogenesis

Table 1
Functions of genes mentioned in the text.
Gene

Full name

ABP1

AUXIN-BINDING PROTEIN 1

Auxin binding protein

Type of molecule

AG

AGAMOUS

MADS-domain transcription
factor

AIL6/PLT3

AINTEGUMENTA-LIKE 6/

Transcription factor

specification of reproductive floral organs and

floral meristem determinacy. Activation of AG
depends on a reversal of PcG repression
mediated by the TFs SEP3 and LFY.
Regulates proliferative growth downstream of

Transcription factor

auxin. Shares overlapping functions in floral

primordium initiation with LFY and ANT.
Regulates proliferative growth downstream of

PLETHORA 3
ANT

AINTEGUMENTA

Function
Extracellular auxin perception in complex with
TMK1. Involved in the maintenance of
anisotropic growth that has to be overcome by
local presence of high auxin to initiate new
floral primordia.
Floral homeotic factor essential for the

AP1

APETALA 1

MADS-domain transcription

auxin. Shares overlapping functions in floral

primordium initiation with LFY and AIL6/PLT3.
Central role in flower identity.

AP3

APETALA 3

factor
MADS-domain transcription

Floral homeotic factor essential for the

factor

specification of petals and stamens. Activation

of AP3 depends on a reversal of PcG
repression mediated by the TFs SEP3 and LFY.

Transcriptional repressor

AUX/IAA factors bind to and repress auxin

response factors (ARFs) in absence of auxin.

CLV1

AUXIN/INDOLE-3-ACETIC
ACID
CLAVATA 1

CLV3

CLAVATA 3

Peptide

Restricts WUS expression to the OC together

with the peptide CLV3.

D6PK

D6 PROTEIN KINASE

AGCVIII protein kinase

Restricts WUS expression to the OC together

with the receptor-like kinase CLV1.

ELA1

EUI-LIKE P450 A1

Cytochrome P450

KNUCKLES

monooxygenase
C2H2-type zinc finger

KTN1

KATANIN 1

protein
Microtubule-severing protein

LCR

LEAF CURLING
RESPONSIVENESS
LEAFY

AUX/IAA

Receptor-like kinase

PIN activation.

KNU

Degrades the phytohormone GA resulting in

derepression of DELLA proteins. DELLA
proteins, together with SPL TFs, activate the
expression of AP1 synergistically with LFY.
Involved in the regulation of floral determinacy.

LFY

MAB4/ENP/NPY1

MACCHI-BOU 4/
ENHANCER OF
PINOID/NAKED PINS IN
YUC MUTANTS 1

Current Opinion in Genetics & Development 2015, 32:1623

Putative F-box protein

Contributes to the formation of anisotropic

cortical microtubules. Local presence of high
levels of auxin has to overcome the anisotropic
growth to initiate new floral primordia.

Transcription factor

Stem cell competence in the SAM requires

repression of LCR by miR394.
Determines floral fate in part by positively

NPH3-like

regulating a central regulator of flower identity

(AP1) and counteracting the negative effect of
GA by activation of ELA1. Shares overlapping
functions in floral primordium initiation with
ANT and AIL6/PLT3. Appears to positively feed
back on auxin signaling, upregulates key auxin
transport regulator PID. Reversal of PcG
repression, together with SEP3, that is required
for the activation of AG and AP3.
Controls reorientation of PIN1 in L1 layer
eventually resulting in an inward auxin
transport

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Early floral development Vaddepalli, Scholz and Schneitz

19

Table 1 (Continued )
Gene
MP/ARF5

Full name

Type of molecule

Function

MONOPTEROS/AUXIN

Auxin response transcription

Activates MAB4. Also activates LFY, ANT and

RESPONSE FACTOR 5

factor

Polycomb group

AIL6/PLT3 that control floral specification and

outgrowth.
Activation of AG and AP3 depends on a

PID

PINOID

AGCVIII protein kinase

reversal of PcG repression mediated by the

TFs SEP3 and LFY. AG replaces the PcG
proteins on KNU promoter in floral
determinacy.
PIN activation.

PIN1

PIN-FORMED 1

Auxin efflux carrier

Required for positioning and initiation of floral

QKY

QUIRKY

PD-localized C2-domain

primordia.
Interacts with the RLK SUB at plasmodesmata.

PcG

transmembrane protein
RIC1

ROP6

ROP-INTERACTIVE CRIB

CRIB-containing ROP

MOTIF-CONTAINING
PROTEIN 1

effector

RHO OF PLANTS 6

Plasma membrane-

of anisotropic growth that has to be overcome

by local presence of high auxin to initiate new
floral primordia.
Regulates a variety of cellular processes.

associated small GTPase

SEP3

SEPALLATA 3

MADS-domain transcription
factor

SPLs

SQUAMOSA PROMOTER

SUB/SCM

BINDING PROTEIN-LIKE
proteins
STRUBBELIG/SCRAMBLED

TIR1/AFB

TRANSPORT INHIBITOR

Required for the control of cell morphogenesis

in L2 layer of floral meristems.
Effector of ROP6. Involved in the maintenance

Involved in the maintenance of anisotropic

growth that has to be overcome by local
presence of high auxin to initiate new floral
primordia.
Interacts with floral homeotic factors.
Activation of the floral patterning genes AG and
AP3 depends on a reversal of PcG repression
mediated by the TFs SEP3 and LFY.
Together with DELLAs, SPLs activate the

Transcription factors

expression of AP1 synergistically with LFY

Atypical receptor-like kinase

Interacts with QKY at plasmodesmata.

F-box protein

Required for the control of cell morphogenesis

in the L2 layer of floral meristems.
Binding of auxin to TIR1/AFB results in the

RESPONSE 1/AUXIN
SIGNALING F-BOX
TMK1

TRANSMEMBRANE

Receptor-like kinase

degradation of AUX/IAA transcriptional

repressors and the concomitant derepression
of ARFs.
Extracellular auxin perception in complex with

WUS

KINASE 1
WUSCHEL

Homeodomain transcription

ABP1.
Mediates stem cell activity in the central zone.

factor
MIR172

MIR394

MICRORNA 172

MICRORNA 394

miRNA

Negative feedback loop with AG in floral

meristem determinacy.
Robustness of the floral meristem determinacy

miRNA

pathway controlled by a feedback loop

between WUS and AG relies on miR172.
The mobile L1-derived miR394 mediates the
repression of LCR required for stem cell
competence in the SAM.

(NPH3)-like genes, including MAB4/ENP/NPY1, that

control the reorientation of PIN1 in the L1 [27 ]. The exact
mechanism of MAB4-mediated PIN1 relocalization
remains to be explored but MAB4 and PIN1 colocalize at
the cell periphery. The data are compatible with the notion
that MAB4-independent convergence of PIN1 polarity is
involved in establishing auxin maxima in the
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L1. The high levels of auxin trigger the MP-mediated local

activation of MAB4 genes, which, in turn, results in the
basipetal reorientation of PIN1 and ultimately in the
establishment of an inward auxin transport.
MP also directly activates three transcription factor genes:
LEAFY (LFY), AINTEGUMENTA (ANT) and
Current Opinion in Genetics & Development 2015, 32:1623

20 Developmental mechanisms, patterning and organogenesis

AINTEGUMENTA-LIKE 6 (AIL6)/PLETHORA 3 (PLT3)

that control floral specification and outgrowth of the
primordium, respectively [28 ]. LFY determines floral fate
[29,30], in part through the direct activation of APETALA1
(AP1), a MADS-domain transcription factor gene with a
central role in floral specification [31]. ANT and
AIL6/PLT3 regulate proliferative growth downstream of
auxin [3234]. A genetic analysis revealed that LFY, ANT
and AIL6/PLT3 share overlapping functions in floral
primordium initiation. Furthermore, LFY appears to positively feed back on auxin signaling as LFY directly binds
to the promoters of many auxin-related genes and upregulates expression of the key auxin transport regulator PID.
The combined results suggested a model for the
coordination of floral primordium initiation, fate specification and outgrowth (Figure 1c). An elevated level of
auxin results in the de-repression of MP, which in turn
directly activates several key transcription factors in-volved
in fate and growth regulation. The positive feed back of
LFY on auxin signaling would lock in the com-mitment to
flower primordium formation [28 ]. Interest-ingly, LFY was
also found to inhibit auxin biosynthesis and its own
expression suggesting a counterbalancing effect on the
stimulation of LFY expression by auxin [35].
Apart from its role in feed back on auxin signaling and in
the activation of floral meristem and floral organ identity
genes, LFY promotes floral fate by repressing signaling
mediated by another phytohormone, gibberellin (GA) [36 ].
Gibberellin promotes the transition from vegeta-tive to
inflorescence development, in part, by activating LFY
expression [37]. However, elevated levels of gibber-ellin in
floral primordia block adoption of floral fate [36 ].
Interestingly, LFY reduces gibberellin levels by directly
activating the expression of the cytochrome P450 gene
EUI-LIKE P450 A1 (ELA1) encoding a gibberellin catabolic enzyme. In the absence of gibberellin, DELLA
proteins can accumulate and, together with SQUAMOSA
PROMOTER BINDING PROTEIN-LIKE (SPL) transcription factors, activate the expression of AP1 synergistically with LFY. Thus, LFY directly activates a central
regulator of flower identity (AP1), counteracts the negative effect of gibberellin, and enhances the responsive-ness
of floral primordia to LFY function (Figure 1c).

Organizing the floral meristem

The floral primordium rapidly develops into a FM. In the
shoot and floral meristems, stem cell homeostasis is
regulated by a negative feedback loop [38,39]. The homeodomain TF gene WUSCHEL (WUS) is expressed in the
OC and mediates stem cell activity in the overlaying central
zone. The stem cells, in turn, restrict WUS ex-pression via
signaling that involves the peptide CLA-VATA 3 (CLV3)
and the receptor-like kinase (RLK) CLV1. Apart from
affecting cytokinin signaling [40], WUS directly activates
transcription of CLV3 [41] and represses expression of
CLV1 [42]. Moreover, WUS
Current Opinion in Genetics & Development 2015, 32:1623

represses the expression of a set of TFs promoting

differentiation [43 ]. Stem cell proliferation can also be
controlled mostly independently of WUS/CLV signaling
[44 ] and stem cell competence in the SAM requires
repression of LEAF CURLING RESPONSIVENESS
(LCR), which is mediated by the mobile L1-derived
miR394 [45 ].
Recent work shed light on the long-standing question of
how WUS exerts its non-autonomous function on stem cell
activity. It was shown that the WUS protein can move from
the OC to the stem cells in the L1 and L2 layers of the
SAM and FM [41]. Movement in the SAM is highly
controlled, essential for WUS function and thus stem cell
maintenance, and occurs via plasmodesmata (PD) [46 ].
Plasmodesmata (PD) are plant-specific, membrane-lined
channels interconnecting most plant cells. They control
passive diffusion or active transport of a variety of cytoplasmic molecules, ranging from metabolites to transcription factors [47].
Current evidence suggests that PD also play a role in the
RLK-mediated inter-cell-layer communication that controls cell morphogenesis of the L2 cells in Arabidopsis
FMs. The anticlinal orientation of cell division planes in the
L2 requires an unknown mobile signal that travels between
cells and whose formation or activity depends on the
atypical LRR-RLK STRUBBELIG (SUB) and the C2domain protein QUIRKY (QKY) [48,49,50 ]. SUB is
present at the plasma membrane but is also found at PD,
where it forms a heteromeric complex with QKY [50 ].
This represents another example for the emerging notion of
a functional convergence of RLK-mediated signal
transduction and PD biology in plant development and
immunity [51,52].

Floral meristem determinacy

In contrast to the indeterminate SAM, which propagates
stem cells and lateral organ production indefinitely, stem
cell activity in the floral meristem ceases after the production of the four types of floral organ primordia. A central
element of floral meristem determinacy control is provid-ed
by a feedback loop in which WUS directly activates the
floral homeotic gene AGAMOUS (AG). AG encodes a
MADS-domain TF involved in floral determinacy and the
specification of reproductive floral organs [53]. Eventually, it indirectly terminates WUS expression and thus
stem cell activity [54,55]. Robustness of this pathway relies
on miR172 function [56]. The mechanism involves
induction of the KNUCKLES (KNU) gene, encoding a
C2H2-type zinc finger protein, by direct binding of AG to
the KNU regulatory region [57]. Induction is delayed by
about two days as repressive H3K27me3 chromatin marks
that have been attached to the KNU locus by Polycomb
group (PcG) complexes are being removed in an AGdependent fashion. The two-day delay in KNU induction
depends on cell cycle progression and on the replacement
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Early floral development Vaddepalli, Scholz and Schneitz

of PcG proteins by AG. The results indicate that floral stem

cells measure developmental time with the help of a
division-dependent epigenetic timer [58 ].
MADS-domain TFs may generally modulate chromatin
accessibility at target loci. A global analysis of chromatin
accessibility and gene expression suggested that the
MADS-domain TFs AP1 and SEP3 act as pioneer pro-teins
that trigger delayed changes in chromatin accessi-bility
[59 ]. Moreover, activation of the floral patterning genes
AP3 and AG depends on a reversal of PcG repres-sion
mediated by the MADS-domain TF SEP3 and LFY [60].

Conclusions
The available data reveal the increasing complexity of the
interactions among hormone signaling, gene regulatory
networks, and cellular behavior governing early floral
development. However, despite impressive progress, our
understanding is still limited. For example the inter-play
between patterning genes and factors directing growth is far
from being understood. Application of genome-wide
approaches with much improved spatial and temporal
resolution or sophisticated genetic screens will continue to
identify novel important factors. Com-puter simulations
will aid in assessing the often non-intuitive network
behavior. Obviously, these regulatory systems are
embedded in a multi-cellular tissue context. Thus, future
progress will also depend on a quantitative morphodynamic
analysis of floral morphogenesis involv-ing 3D imaging at
cellular resolution, combined with computer modeling of
growth processes. This approach resulted in new concepts
in, for example, sepal and petal morphogenesis [61 ,62],
and revealed the interplay be-tween mechanics, cell
geometry, and growth patterns in the embryo [63 ].

Acknowledgments
We thank Doris Wagner, Jan Lohmann and Teva Vernoux for comments.
Research in the Schneitz lab is funded by the German Research Council (DFG)
(SCHN 723/7-1 and SFB924 TP A2).

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Papers of particular interest, published within the period of review,
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of special interest
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Current Opinion in Genetics & Development 2015, 32:1623