Download Formative Cell Divisions: Principal Determinants of Plant

Michalina Smolarkiewicz1 and Pankaj Dhonukshe1,2,3,*
1
Department of Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands
Department of Plant Systems Biology, VIB, B-9052, Ghent, Belgium
3
Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052, Ghent, Belgium
*Corresponding author: E-mail, [email protected]; Fax, +32-9-3313809
(Received October 7, 2012; Accepted December 6, 2012)
2
Formative cell divisions utilizing precise rotations of cell division planes generate and spatially place asymmetric daughters to produce different cell layers. Therefore, by shaping
tissues and organs, formative cell divisions dictate multicellular morphogenesis. In animal formative cell divisions, the
orientation of the mitotic spindle and cell division planes
relies on intrinsic and extrinsic cortical polarity cues. Plants
lack known key players from animals, and cell division planes
are determined prior to the mitotic spindle stage. Therefore,
it appears that plants have evolved specialized mechanisms
to execute formative cell divisions. Despite their profound
influence on plant architecture, molecular players and cellular
mechanisms regulating formative divisions in plants are not
well understood. This is because formative cell divisions in
plants have been difficult to track owing to their submerged
positions and imprecise timings of occurrence. However, by
identifying a spatiotemporally inducible cell division plane
switch system applicable for advanced microscopy techniques, recent studies have begun to uncover molecular modules and mechanisms for formative cell divisions. The
identified molecular modules comprise developmentally triggered transcriptional cascades feeding onto microtubule
regulators that now allow dissection of the hierarchy of the
events at better spatiotemporal resolutions. Here, we survey
the current advances in understanding of formative cell divisions in plants in the context of embryogenesis, stem cell
functionality and post-embryonic organ formation.
Abbreviations: ARF, auxin-responsive factor; AUX/IAA,
AUXIN/INDOLE-3-ACETIC ACID (repressor proteins); CEI,
cortex/endodermal initial; CLASP, CLIP-associated protein;
Epi/LRC, epidermis/lateral root cap; MAP65, microtubuleassociated proteis 65; MT, microtubule; PIN, Pin-formed
(auxin efflux carrier); PLT, PLETHORA; PPB, pre-prophase
band; QC, quiescent center; SCR, SCARECROW; SHR,
SHORTROOT.
A relay of coordinated oriented cell divisions involving precise
cell division plane switches gradually transforms the fertilized
egg cell into an embryo by determining the fates and positions
of cells, patterning tissues and creating organs. Therefore,
oriented cell divisions form ‘principal determinants’ of multicellular morphogenesis. Symmetric cell divisions with median
cell division planes create two daughters of identical sizes
and/or fates. This allows amplification of cell populations.
Asymmetric cell divisions, on the other hand, with median or
offset division planes, generate daughters of non-identical sizes
and/or fates. This allows creation of cellular heterogeneity
(Scheres and Benfey 1999, Rasmussen et al. 2011a).
Active control of mitotic division planes is essential to
numerous processes in animals, such as embryogenesis
(Castanon and González-Gaitán 2011), gastrulation (Gong
et al. 2004), neural tube morphogenesis (Quesada-Hernández
et al. 2010) and organ development (Baena-López et al. 2005).
In dividing animal cells, the orientation of cell division relies on
intrinsic (Cowan and Hyman 2004) and extrinsic cortical polarity cues (Siller and Doe 2009), which specify the orientation of
the mitotic spindle. In many instances, astral microtubules
(MTs) originating from the spindle pole navigate their growth
trajectories in relation to the cortical polar coordinates such
as partitioning-defective proteins to position the division
plane during asymmetric cell divisions (Knoblich 2010). Cell
division planes in plants are specified prior to mitosis by transformation of a cortical MT array into a so-called pre-prophase
band (PPB) (Pickett-Heaps and Northcote 1966, Dhonukshe
and Gadella 2003). During plant cytokinesis, a new wall partitions the parental cell into two daughters from within, and
attaches to the parental cell cortex at the position previously
occupied by the PPB. A variety of observations indicate that
the cortical division site remains marked throughout mitosis
and cytokinesis after the PPB has disassembled (Nogami and
Mineyuki 1999, Smith 2001, Müller et al. 2009). Recent work
has identified positive and negative markers for the cortical
division site and has implicated them in conveying a memory
from the PPB position to guide the cell plate (Müller et al. 2006,
Plant Cell Physiol. 54(3): 333–342 (2013) doi:10.1093/pcp/pcs175, available FREE online at www.pcp.oxfordjournals.org
! The Author 2012. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.
All rights reserved. For permissions, please email: [email protected]
Plant Cell Physiol. 54(3): 333–342 (2013) doi:10.1093/pcp/pcs175 ! The Author 2012.
Editor-in-Chief’s choice
Keywords: Arabidopsis thaliana Auxin Cell division plane
Formative cell divisions Microtubule arrays Transcription factors.
Introduction
Special Focus Issue – Mini Review
Formative Cell Divisions: Principal Determinants of
Plant Morphogenesis
333
M. Smolarkiewicz and P. Dhonukshe
Azimzadeh et al. 2008, Van Damme 2009, Wright et al. 2009).
Most of these proteins follow the PPB MTs in terms of
their spatiotemporal localizations and seem to operate downstream (Hoshino et al. 2003, Vanstraelen et al. 2006, Walker
et al. 2007, Müller et al. 2009, Rasmussen et al. 2011b,
Van Damme et al. 2011), attesting to the prime importance
of PPB positioning.
Plant cells are surrounded by the rigid cell walls and, as a
result, they are immobile. Descendant cells are placed next
to the mother cell and remain there throughout their lifespan. The orientation of the cell division plane is critical as it
determines not only the positions of daughter cells but also
their developmental fates. Therefore, the directions in which
plant cells divide by positioning the cell wall partitions
determine cell layer creation, tissue organization, organ formation and plant architecture. Many of the plant organs
display a radial cell layer pattern. To create successive
radial layers, cell divisions have to be oriented parallel to
the surface (‘periclinal’). Asymmetric periclinal cell divisions,
where daughter cells acquire distinct identities, have been
termed ‘formative divisions’ (Gunning 1978). Thus, formative
cell divisions generate concentric cell layers and proliferative
cell divisions propagate already formed layers. Most of formative divisions occur at early embryo stages when the body
plan is established (Jürgens et al. 1995, De Smet and
Beeckman 2011), and others take place when lateral organs
are launched (De Smet 2012). Formative divisions involving
precise cell division plane switches are key aspects of plant
stem cells, as they allow stem cells to self-renew and to
produce daughter cells of different fates for creating new
cell layers (Dolan et al. 1993). Here we review recent findings
concerning cellular and molecular aspects of formative cell
divisions in plants with respect to important developmental
contexts.
dermatogen stage, a single outer layer termed the protoderm
is produced. By utilizing formative divisions, it later produces
the epidermis of the plant. Radial periclinal divisions in the
proembryo further generate the ground and vascular progenitors, whereas the uppermost suspensor cells become
the hypophysis (De Smet et al. 2010a, Peris et al. 2010).
Hypophysis division generates the lens-shaped cell as the
progenitor of the quiescent center (QC). The QC with surrounding stem cells maintains the root stem cell niche.
At the heart stage, proliferation of cells in the upper half
of the embryo gives rise to cotyledon primordia which is the
first appearance of bilateral symmetry (Jürgens et al. 1997,
Jeong et al. 2011). In 10 days the embryo consists of about
20,000 cells, is about 0.5 mm in length and has developed a
body plan similar in miniature to that of the Arabidopsis
seedling. The majority of formative divisions occur at early
embryo stages (Fig. 1A), and they are crucial for establishment of the plant body plan (Jürgens et al. 1995, De Smet
Embryonic Formative Cell Divisions
During plant embryogenesis, a relay of coordinated oriented
cell divisions gradually transforms the zygote into a mature
embryo (Peris et al. 2010, Jeong et al. 2011). In a model plant,
Arabidopsis thaliana, after fertilization the zygote undergoes
the first asymmetric division to produce an apical cell which
gives rise to the bulk of the embryo proper and a basal cell
which gives rise to the suspensor connecting the embryo
to the nutrient-supplying maternal tissues. The apical cell
divides first periclinally and the basal cells divide anticlinally
to proceed towards the 4-cell stage. The basal cells continue
dividing in anticlinal orientations to increase the cell number,
whereas the apical cells follow a choreographed oriented
cell division program to establish initial embryonic domains
comprising cells of different shapes, fates and positions. The
embryo passes through successive developmental stages
called the dermatogen stage, the globular stage, the transition
stage, the heart stage and the torpedo stage. At the
334
Fig. 1 Typical formative cell divisions that occur during plant morphogenesis. (A) In early embryogenesis, formative cell divisions involving a relay of cell division plane rotations (marked by the red dashed
line) shape the apical part of the embryo. (B) Post-embryonic lateral
root formation (B; top box) and creation of a new cell layer in the root
apical meristem (B; bottom box) also require a tightly orchestrated
series of periclinal and anticlinal divisions (green arrows) to generate
and sustain the final root layout. En, endodermis; C, cortex; E, epidermis; LRC, lateral root cap.
Plant Cell Physiol. 54(3): 333–342 (2013) doi:10.1093/pcp/pcs175 ! The Author 2012.
Formative cell divisions
and Beeckman 2011). Randomization of cell division planes
in plant embryos leads to drastic morphogenetic defects
including embryo lethality (Berleth and Jürgens 1993,
Torres-Ruiz and Jürgens 1994, Traas et al. 1995, Camilleri
et al. 2002).
Experimental data indicate that the plant-specific signaling
molecule auxin has a profound influence on plant embryogenesis and post-embryonic development (Jürgens et al. 1991,
Reinhardt et al. 2000, Friml et al. 2003, Furutani et al. 2004,
Dharmasiri et al. 2005a). Auxin controls expression of
auxin-dependent genes through auxin signaling pathways.
Auxin signaling involves the activation of transcription factors
known as auxin-responsive factors (ARFs) which induce the
expression of auxin-dependent genes (Ulmasov et al. 1999,
Weijers et al. 2005, Guilfoyle and Hagen 2007). ARF activity is
repressed by the AUXIN/INDOLE-3-ACETIC ACID (AUX/IAA)
repressor proteins (Rouse et al. 1998, Worley et al. 2000,
Dharmasiri and Estelle 2002). Auxin binds to its intracellular
auxin receptor ‘transport inhibitor response 1 (TIR1) protein,
the F-box component of the SCFTIR1 E3 ubiquitin ligase complex. TIR1 ubiquitinates AUX/IAA repressors and triggers their
degradation, thus releasing the inhibition of ARF transcriptional
activity (Dharmasiri et al. 2005b). The presence of 23 ARFs
and 29 AUX/IAAs in Arabidopsis represents a complex matrix
configuration of the auxin signaling pathway (Guilfoyle and
Hagen 2007, Lokerse and Weijers 2009). Due to their vast
number and the possibility of multiple pairwise interactions
between ARFs and AUX/IAAs, the molecular details of their
precise spatiotemporal action patterns remain unclear.
Nevertheless, the importance of TIR1-based auxin signaling
for plant development has been suggested as quadruple tir1related mutants display dramatic patterning defects in embryo
development (Dharmasiri et al. 2005a, Calderon-Villalobos et al.
2010). As auxin amounts appear to translate into auxin signaling, many aspects of auxin action seem to depend on its spatial
distribution patterns within plant tissues, where it forms local
maxima and minima (Friml et al. 2003, Dhonukshe et al. 2008,
Sorefan et al. 2009). In order to create gradients, auxin biosynthesis, transport and conjugation need to be spatiotemporally
regulated. Auxin biosynthesis is restricted to certain plant
regions and then it is distributed in a controlled manner.
This spatial auxin distribution is established mainly by the
directional cell to cell transport mediated by action of the
polar-localized auxin efflux carrier PIN proteins (Friml et al.
2003). The PIN family consists of eight members (PIN1–PIN8)
(Paponov et al. 2005). PIN1, 3, 4 and 7 were shown to be essential for embryogenesis as pin1/pin3/pin4/pin7 quadruple
mutants are defective in the overall establishment of apical–
basal polarity (Benková et al. 2003, Friml et al. 2003, Blilou
et al. 2005). Single pin mutants can complete normal embryo
development, indicating their functional redundancy. Also a
mutant for GNOM, which is crucial for endosomal recycling
and polar localization of PIN, results in impaired asymmetric
division of the zygote and embryo lethality (Mayer et al. 1991,
Mayer et al. 1993).
Auxin-responsive transcription factor MONOPTEROS
(MP/ARF5) and its repressor BODENLOS (BDL/IAA12) are
important for early embryogenesis (Berleth and Jürgens 1993,
Hardtke and Berleth 1998). In a fraction of loss-of-function mp
and gain-of-function bdl mutants, orientation of the division
plane of the apical daughter of the zygote is affected. Moreover,
the uppermost suspensor cell in these mutants fails to
become the founder cell of the primary root meristem, resulting
in a rootless phenotype of the seedlings (Hamann et al.
1999, Hamann et al. 2002, Weijers et al. 2006). Recently, two
target of monopteros (TOM) transcription factors, TOM5
and TOM7, were shown to act downstream of MP in the
root initiation program (Schlereth et al. 2010). Interestingly,
MP was shown to influence the direction of auxin flow to the
hypophysis precursor via its effect on PIN1 expression and
PIN1-mediated polar auxin transport, highlighting the feedback
loops between auxin signaling and auxin transport (Weijers
et al. 2006).
Genetic studies in Arabidopsis have identified a variety of
other molecular factors such as type 2C protein phosphatases
POLTERGEIST (POL) and POLTERGEIST-LIKE1 (PLL1) (Song
and Clark 2005, Gagne et al. 2008, Gagne and Clark 2010)
that are required for orientation and execution of formative
cell divisions. In the apical hypophyseal daughter cell, POL/PLL1
were shown to induce expression of the WUS
homeobox-containing (WOX) transcription factor WOX5
(Song et al. 2008) that is essential for maintenance of the
root stem cell niche (Sarkar et al. 2007). Importantly, double
pol/pll1 mutants show loss of asymmetry during the procambial and hypophyseal cell divisions, leading to defects in root
meristem organization (Song et al. 2006, Song et al. 2008). In
addition, embryo patterning at early embryonic stages is regulated by spatially restricted expression of several other transcription factors. In early embryo development, members of
the WOX transcription factor family, WOX2, 8 and 9, exhibit
different expression patterns in apical and basal cell lineages
and act in a partially redundant manner for embryo patterning.
A fraction of wox8/wox9 double mutants is defective in executing vertical rotation of the division plane at the 1-cell embryo
stage. A subset of embryos continues to develop into finger-like
structures and further development of the embryo is arrested
(Haecker et al. 2004, Wu et al. 2007, Breuninger et al. 2008).
Recently, the GATA-type transcription factor HANABA
TARANU (HAN) has been shown to be required for maintaining the functional boundary between proembryo and
suspensor. han mutant cells from the lower tier of the proembryo acquire the developmental identity of a suspensor.
Interestingly, han mutant embryos exhibit an apical shift in
the expression pattern of PINs (Nawy et al. 2010), suggesting
that its defects are related to auxin homeostasis.
Despite the well recognized role of auxin gradients and identification of a set of transcription factors involved in formative
cell divisions during embryogenesis, details of the molecular
pathways and mechanisms driving rotation of cell division
planes for formative cell divisions are lacking.
Plant Cell Physiol. 54(3): 333–342 (2013) doi:10.1093/pcp/pcs175 ! The Author 2012.
335
M. Smolarkiewicz and P. Dhonukshe
Organization of Root Meristem Stem
Cell Niche
Transverse sections of the Arabidopsis primary root reveal that
the organization and number of cells is remarkably maintained.
The layout of the root is highly ordered, consisting of concentric, single-layer cylinders of epidermal, cortical, endodermal,
pericycle and vascular tissues (Dolan et al. 1993). Continuous
apical growth of the root is maintained by a group of mitotically
silent QC cells surrounded by mitotically active stem cells such
as cortex/endodermal initials (CEIs), epidermis/lateral root cap
(Epi/LRC) stem cells or columella stem cells (Aida et al. 2004,
Campilho et al. 2006). A spatially controlled switch of the cell
division plane is essential to drive a relay of anticlinal and periclinal divisions of ECIs and Epi/LRC stem cells (Fig. 1B, bottom)
contributing to the final root layout.
Members of the PLETHORA (PLT) transcription factor
family control activity of the root stem cell niche (Aida et al.
2004). plt1/plt2/plt3 mutants lack a lateral root cap cell layer,
suggesting impaired formative cell division of Epi/LRC stem
cells (Galinha et al. 2007). plt1/plt2 mutants display reduced
frequency of the anticlinal to perclinal division plane switch in
Epi/LRC stem cells. As a result, they develop fewer LRC layers.
Induction of PLT1 or PLT2 in the plt1/plt2 mutant rescues
these defects, suggesting their functional redundancy
(Dhonukshe et al. 2012). PLT executes its effects via auxin signaling pathway-dependent expression of MT regulators
MAP65-1 and MAP65-2 (microtubule-associated proteins 65)
(Dhonukshe et al. 2012). In accordance with this, double
map65-1/map65-2 mutants display a reduced number of periclinal divisions in root Epi/LRC stem cells, resulting in a reduced
number of LRC layers (Sasabe et al. 2011). Further, the influence
of PLT1 and PLT2 on cell division plane orientation seems to
be auxin related as their expression patterns largely overlap
with that of the auxin activity gradient (Galinha et al. 2007).
In plants, MAP65s have been shown to control the bundling
status of MTs (Chang-Jie and Sonobe 1993, Smertenko et al.
2004). In Nicotiana tabacum, bundling activity of MAP65 is
regulated by the MAPK (mitogen-activated protein kinase)
NRK1/NTF6 (Sasabe et al. 2006). Moreover MAP65 phosphorylation appears crucial for cell cycle progression and phragmoplast expansion. Interestingly, plant MAP65 bundling activity
is not regulated by CDK (cyclin-dependent kinase), although
CDK is the major regulator of MAP65 activity in animals
(Mollinari et al. 2002, Sasabe et al. 2006). Recently MAP65-1
and MAP65-2 were shown to contribute to cell division plane
rotation by influencing CLASP (CLIP-associated protein) localization (Dhonukshe et al. 2012). CLASP is an MT-associated
protein that seems to stabilize MTs (Ambrose et al. 2007).
CLASP is thought to influence cell expansion (Ambrose et al.
2007) as well as cell division (Ambrose et al. 2007, Kirik et al.
2007) and clasp-1 mutants exhibit significant dwarfing during
development (Ambrose et al. 2007). Polyhedral plant cells
possess sharp top/bottom corners and soft lateral corners
that allow transversal but prohibit longitudinal MT array
336
organization. Interestingly, in cells competent to undergo
periclinal division, CLASP localizes preferably to sharp cell
edges, whereas in those cells that have undergone periclinal
division or those that are undergoing anticlinal cell divisions
CLASP shows lateral localization (Ambrose et al. 2011,
Dhonukshe et al. 2012). Computational analyses revealed that
loading of CLASP at the sharp top/bottom corners allows
MT bypass from the lateral to the top/bottom cell sides for
rotation of the MT array from the transversal to longitudinal
direction, and this then switches the cell division plane
(Dhonukshe et al. 2012). Importantly, MAP65-labeled and
bundled MTs have been shown to contribute to the switch
in CLASP localization from soft lateral to sharp top/bottom
cell edges (Dhonukshe et al. 2012). What cellular landmarks
the MTs follow and how CLASP is recruited to selective
cell edges remain unclear, but MAP65 seems to play an instructive role via CLASP delivery and/or persistence at certain cell
edges. Thus the discovery of this PLT–auxin–MAP65–CLASP
module opens the door to test its relevance for other types
of formative cell divisions and to identify players and mechanisms that operate for their execution.
It has been shown that the activity of two GRAS-type transcription factors, SCARECROW (SCR) and SHORTROOT (SHR),
control the potential of endodermis/cortex initials by organizing formative cell divisions (Benfey et al. 1993, Scheres et al.
1995, Di Laurenzio et al. 1996, Sabatini et al. 2003). Mutations in
SCR and SHR genes result in formation of a single ground tissue
layer. In scr mutants, the single tissue layer has attributes characteristic of both cortex and endodermis (Scheres et al. 1995, Di
Laurenzio et al. 1996). On the other hand, in shr mutants, the
single layer of ground tissue is deprived of endodermal determinants but still acquires the attributes of cortex (Benfey et al.
1993, Helariutta et al. 2000). Overexpression of SHR triggers
additional layer formation, indicating that SHR is essential for
formative cell divisions (Helariutta et al. 2000). Interestingly,
SHR is transcribed in the stele, but the SHR protein moves to
endodermis/cortex initials. There it binds to SCR and induces
the asymmetric periclinal divisions to generate endodermis and
cortex tissues (Helariutta et al. 2000, Heidstra et al. 2004,
Gallagher et al. 2004, Cui et al. 2007).
SHR is a positive regulator of SCR expression (Helariutta
et al. 2000), SCR limits radial SHR movement by binding
and diverting it to the nucleus (Cui et al. 2007) and SCR
activity is potentially inhibited by its binding to plant
RETINOBLASTOMA-RELATED (RBR) protein which is one of
the factors regulating cell cycle progression (Wildwater et al.
2005, Cruz-Ramı́rez et al. 2012). In Arabidopsis, RBR inactivation is presumably mediated by CYCLIND6;1 (CYCD6;1) which
is a transcriptional target of SHR (Sozzani et al. 2010). An
enhanced amount of auxin as well as SHR and SCR activity
are both required for CYCD6;1 expression (Cruz-Ramı́rez
et al. 2012). Thus a delicate interplay between SHR–SCR
activation and inactivation events, cell cycle progression and
protein degradation linked to the lateral auxin gradients and
the radial SHR gradients restricts formative cell divisions to the
Plant Cell Physiol. 54(3): 333–342 (2013) doi:10.1093/pcp/pcs175 ! The Author 2012.
Stem cell
niche
Transcription factor
WOX2
Transcription factors
Microtubule-associated
proteins
Microtubule-associated
protein
Transcription factor
Transcription factor
PLT1, 2, 3
MAP65-1, 2
CLASP
SCR
SHR
Transcription factor
Type 2C protein
phosphatases
POL/PLL1
HAN
Transcription factor and
repressor protein
MP and BDL
Transcription factors
Auxin efflux carriers
PIN1, 3, 4, 7
WOX8, 9
ADP-ribosylation
factor-guanine
nucleotide exchange
factor
GNOM
Embryo
Molecule
Gene
System
Single cell layer between the epidermis
and pericycle lacking markers for
endodermis
Single cell layer between the epidermis
and pericycle with markers of both
cortex and endodermis
Cell division abnormalities and reduced
number of periclinal divisions in Epi/
LRC stem cells
Cell division abnormalities and reduced
number of periclinal divisions in Epi/
LRC stem cells
Rootless phenotype; reduced number of
LRC layers
Abnormal early embryo morphology;
arrest of hypophysis development
Aberrant apical cell division; in basal lineage: irregular cell division planes or
enlarged, misshapen cells
Abnormal apical development recovered
at mid-globular stage
Seedling lethal, develop files of
cortex-like, undifferentiated cells; fail to
develop shoot meristem
Rootless phenotype; failed hypophysis
specification
Multiple early embryo defects
Multiple early embryo defects
Mutant phenotype
Table 1 Genes known to regulate plant asymmetric divisions in diverse developmental contexts
Generation and cell fate determination
of cortex and endodermal cells
Generation of cortex and epidermal
cells
Cell division plane rotation in epidermis/lateral root cap stem cells
Cell division plane rotation in epidermis/lateral root cap stem cells
Activity of root stem cell niche; periclinal division of Epi/LRC stem cells
Maintenance of boundary between
proembryo and suspensor
Early embryo pattering and establishment of apical–basal polarity
Early embryo development
Meristem formation; asymmetry of procambial and hypophyseal cells
division
Apical–basal pattern formation; division
of apical cell and hypophysis
Early embryo patterning and establishment of apical–basal polarity
Establishment of apical–basal body axis
Role
Reference
(continued)
Benfey et al. (1993), Helariutta et al.
(2000); Cruz-Ramı́rez et al. (2012)
Scheres et al. (1995); Di Laurenzio
et al. (1996); Cruz-Ramı́rez
et al. (2012)
Ambrose et al. (2011); Dhonukshe
et al. (2012)
Dhonukshe et al. (2012)
Aida et al. (2004); Galinha et al. (2007);
Dhonukshe et al. (2012)
Nawy et al. (2010)
Wu et al. (2007); Breuninger et al.
(2008)
Haecker et al. (2004)
Song et al. (2006); Gagne et al. (2008);
Song et al. (2008); Gagne and
Clark (2010)
Berleth and Jürgens (1993); Hardtke
and Berleth (1998); Hamann et al.
(1999); Hamann et al. (2002);
Weijers et al. (2006)
Benková et al. (2003); Friml et al.
(2003); Blilou et al. (2005)
Mayer et al. (1991, 1993)
Formative cell divisions
Plant Cell Physiol. 54(3): 333–342 (2013) doi:10.1093/pcp/pcs175 ! The Author 2012.
337
338
De Smet et al. (2008, 2010)
Initiation step
Receptor-like kinase
ACR4
Increased number of lateral root primodia; disrupted spacing
Robert and Offringa (2008); Kleine-Vehn
et al. (2009)
Initiation step
AGC kinase
PID
Reduced number of lateral roots
Benková et al. (2003)
Initiation and patterning
Auxin efflux carrier
PIN
combinations
Reduced number of lateral roots
Geldner et al. (2004); Kleine-Vehn et al.
(2008)
Initial asymmetric cell divisions
ADP-ribosylation
factor-guanine
nucleotide exchange
factor
GNOM
Reduced number of lateral roots
Fukaki et al. (2002, 2005)
Initiation and emergence steps
Repressor protein
IAA14/SLR-1
Lack of lateral root
DiDonato et al. (2004)
Maintenance of xylem pericycle cells in
mitotis-competent state
Lack of lateral roots
Nuclear protein
ALF4
Lateral
root
Table 1 Continued
Molecule
Gene
System
Mutant phenotype
Role
Reference
M. Smolarkiewicz and P. Dhonukshe
stem cell niche (Cruz-Ramı́rez et al. 2012). Details of this
module need to be investigated further to elucidate the
molecular players acting downstream of SCR/SHR and
auxin activity that influence the MT cytoskeleton to execute
formative cell divisions.
Formation of Lateral Roots
Formation of lateral roots requires cell dedifferentiation
followed by coordinated divisions in order to produce new
cell types. Lateral roots are initiated in the pericycle xylem
poles (Blakely et al. 1982, Laskowski et al. 1995, Péret et al.
2009, De Smet 2012). These cells maintain the ability to
divide outside the root meristem by continuous expression
of ALF4 protein (ABERRANT LATERAL ROOT FORMATION
4), which is required to keep cells in a mitosis-competent
state (DiDonato et al. 2004). A limited number of the xylem
pericycle cells undergo auxin-dependent priming and gain
pericycle founder cell identity. Lateral root fate can be induced
in every xylem pericycle cell by an elevated level of auxin
(Dubrovsky et al. 2008), but for certain reasons only a limited
number of cells gain founder cell identity. Regular distribution
of lateral roots along the main root indicates a strict spatiotemporal control of lateral root initiation events (De Smet et al.
2007, Lucas et al. 2008). Indeed, it has been shown that oscillation of the auxin level is sufficient for initiation of xylem cells
(De Smet et al. 2007, Moreno-Risueno et al. 2010).
Once specified, a subset of founder cells undergoes a series
of anticlinal and periclinal formative divisions to give rise to
lateral root primodia as described in Fig. 1B (top). Here, one of
the most important players seems to be the ARF SOLITARY
ROOT 1 (SLR1/IAA14). It has been shown that pericycle founder cells in gain-of-function slr-1 mutants fail to undergo
formative divisions to produce lateral root primodia (Fukaki
et al. 2002, Fukaki et al. 2005). Recently, SLR1 has been found
to act upstream of two ARFs, ARF7 and ARF19, and two
LATERAL ORGAN BOUNDRIES-DOMAIN 16 (LBD16) and
LBD29 proteins to control lateral root formation (Okushima
et al. 2007). Constitutively active iaa14/slr-1 mutants and
inactive arf7/arf19 mutants completely lack lateral roots, indicating a master regulatory function for the SLR1–ARF7–ARF19
module (Fukaki et al. 2002, Okushima et al. 2005). Multiple
mutants in PIN genes (Benková et al. 2003), as well as mutants
for PIN-trafficking regulators GNOM (Geldner et al. 2004,
Kleine-Vehn et al. 2008) or PINOID kinase (Robert and
Offringa 2008, Kleine-Vehn et al. 2009), display lateral root
abnormalities linked to the inability to execute formative divisions. Interestingly, gnom and slr-1 mutants lack the expression
of the receptor-like kinase ARABIDOPSIS CRINKLY 4 (ACR4)
which in the wild type is transcribed specifically in the small
daughter cells after the first asymmetric pericycle cell division
and then its expression expands to the adjacent small daughter
cells from the second asymmetric cell division (De Smet et al.
2008). ACR4 is required to coordinate pericycle cell divisions
Plant Cell Physiol. 54(3): 333–342 (2013) doi:10.1093/pcp/pcs175 ! The Author 2012.
Formative cell divisions
during lateral root initiation. It is considered to suppress cell
divisions in pericycle cells surrounding the lateral root. In acr4
mutants, lateral root primodia are initiated close to or even
fused with each other, and often form stretches of two-layered
pericycle (De Smet et al. 2008). Importantly, auxin treatment of
the slr-1 mutant restores ACR4 expression which is limited to
stretches of dividing pericycle cells (De Smet et al. 2010b).
However, the mechanisms of how the auxin gradient and
auxin signaling launch the lateral root formation program
and how it is coordinated with rotation of the division plane
still remain unknown.
Perspectives
In recent years, a great deal of efforts have been made towards
gaining a better understanding of the mechanism underlying
formative divisions in various developmental contexts in
plants. A set of transcription factors and the plant hormone
auxin were identified to play key regulatory roles for formative
cell divisions. However, a picture of hierarchical events beginning from a developmental trigger, passing through the transcriptional programs and feeding onto MT cytoskeleton
reorganization for determining and executing formative cell
divisions is far from being complete. A delicate and tangled
interplay between the transcription factors, auxin and a vast
number of auxin signaling components, and cytoskeletal
regulators certainly poses big challenges in unraveling the
details of the formative cell division machinery within the
plant kingdom. Recent identification of the PLT–auxin–
MAP65–CLASP module provides us with a roadmap towards
identifying similar and diverse modules that act at different
plant regions, which will lead towards a better understanding
of the formative cell divisions.
Funding
This work was supported by the Utrecht University
Starting Independent Investigator Grant and Netherlands
Organisation for Scientific Research’s VIDI grant to P.D.
Acknowledgments
We apologize to the colleagues whose work could not be cited
due to the space constraints.
References
Aida, M., Beis, D., Heidstra, R., Willemsen, V., Blilou, I., Galinha, C. et al.
(2004) The PLETHORA genes mediate patterning of the
Arabidopsis root stem cell niche. Cell 119: 109–120.
Ambrose, C., Allard, J.F., Cytrynbaum, E.N. and Wasteneysa, G.O.
(2011) A CLASP-modulated cell edge barrier mechanism drives
cell-wide cortical microtubule organization in Arabidopsis.
Nat. Commun. 2: 430.
Ambrose, C., Shoji, T., Kotzer, A.M., Pighin, J.A. and Wasteneys, G.O.
(2007) The Arabidopsis CLASP gene encodes a microtubuleassociated protein involved in cell expansion and division. Plant
Cell 19: 2763–2775.
Azimzadeh, J., Nacry, P., Christodoulidou, A., Drevensek, S.,
Camilleri, C., Amiour, N. et al. (2008) Arabidopsis TONNEAU1 proteins are essential for preprophase band formation and interact
with centrin. Plant Cell 20: 2146–2159.
Baena-López, L.A., Baonza, A. and Garcı́a-Bellido, A. (2005) The orientation of cell divisions determines the shape of Drosophila organs.
Curr. Biol. 15: 1640–1644.
Benfey, P.N., Linstead, P.J., Roberts, K., Schiefelbein, J.W., Hauser, M.T.
and Aeschbacher, R.A. (1993) Root development in Arabidopsis:
four mutants with dramatically altered root morphogenesis.
Development 119: 57–70.
Benková, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D.,
Jürgens, G. et al. (2003) Local, efflux-dependent auxin gradients as a
common module for plant organ formation. Cell 115: 591–602.
Berleth, T. and Jürgens, G. (1993) The role of the monopteros gene in
organizing basal development in the Arabidopsis embryo.
Development 118: 575–587.
Blakely, L.M., Durham, M., Evans, T.A. and Blakely, R.M. (1982)
Experimental studies on lateral root formation in radish seedling
roots. General methods, developmental stages, and spontaneous
formation of laterals. Bot. Gaz. 143: 341–352.
Blilou, I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I., Friml, J. et al.
(2005) The PIN auxin efflux facilitator network controls growth and
patterning in Arabidopsis roots. Nature 433: 39–44.
Breuninger, H., Rikirsch, E., Hermann, M., Ueda, M. and Laux, T. (2008)
Differential expression of WOX genes mediates apical–basal axis
formation in the Arabidopsis embryo. Dev. Cell 14: 867–876.
Calderon-Villalobos, L.I., Tan, X., Zheng, N. and Estelle, M. (2010) Auxin
perception—structural insights. Cold Spring Harb. Perspect. Biol. 2:
a005546.
Camilleri, C., Azimzadeh, J., Pastuglia, M., Bellini, C., Grandjean, O. and
Bouchez, D. (2002) The Arabidopsis TONNEAU2 gene encodes
a putative novel protein phosphatase 2A regulatory subunit essential for the control of the cortical cytoskeleton. Plant Cell 14:
833–845.
Campilho, A., Garcia, B., Toorn, H.V., Wijk, H.V. and Scheres, B. (2006)
Time-lapse analysis of stem-cell divisions in the Arabidopsis thaliana root meristem. Plant J. 48: 619–627.
Castanon, I. and González-Gaitán, M. (2011) Oriented cell division in
vertebrate embryogenesis. Curr. Opin. Cell Biol. 23: 697–704.
Chang-Jie, J. and Sonobe, S. (1993) Identification and preliminary
characterization of a 65 kDa higher-plant microtubule-associated
protein. J. Cell Sci. 105: 891–901.
Cowan, C.R. and Hyman, A.A. (2004) Asymmetric cell division in
C. elegans: cortical polarity and spindle positioning. Annu. Rev.
Cell Dev. Biol. 20: 427–453.
Cruz-Ramı́rez, A., Dı́az-Triviño, S., Blilou, I., Grieneisen, V.A., Sozzani, R.,
Zamioudis, C. et al. (2012) A bistable circuit involving
SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division. Cell 150: 1002–1015.
Cui, H., Levesque, M.P., Vernoux, T., Jung, J.W., Paquette, A.J.,
Gallagher, K.L. et al. (2007) An evolutionarily conserved mechanism
delimiting SHR movement defines a single layer of endodermis in
plants. Science 316: 421–425.
De Smet, I. (2012) Lateral root initiation: one step at a time.
New Phytol. 193: 867–873.
Plant Cell Physiol. 54(3): 333–342 (2013) doi:10.1093/pcp/pcs175 ! The Author 2012.
339
M. Smolarkiewicz and P. Dhonukshe
De Smet, I. and Beeckman, T. (2011) Asymmetric cell division in land
plants and algae: the driving force for differentiation. Nat. Rev. Mol.
Cell. Biol. 12: 177–188.
De Smet, I., Lau, S., Mayer, U. and Jürgens, G. (2010a) Embryogenesis—
the humble beginnings of plant life. Plant J. 61: 959–970.
De Smet, I., Lau, S., Voss, U., Vanneste, S., Benjamins, R.,
Rademacher, E.H. et al. (2010b) Bimodular auxin response controls
organogenesis in Arabidopsis. Proc. Natl Acad. Sci. USA 107:
2705–2710.
De Smet, I., Tetsumura, T., De Rybel, B., Frey, N.F., Laplaze, L.,
Casimiro, I. et al. (2007) Auxin-dependent regulation of lateral
root positioning in the basal meristem of Arabidopsis.
Development 134: 681–690.
De Smet, I., Vassileva, V., De Rybel, B., Levesque, M.P., Grunewald, W.,
Van Damme, D. et al. (2008) Receptor-like kinase ACR4 restricts
formative cell divisions in the Arabidopsis root. Science 322:
594–597.
Dharmasiri, N., Dharmasiri, S. and Estelle, M. (2005b) The F-box protein TIR1 is an auxin receptor. Nature 435: 441–445.
Dharmasiri, N., Dharmasiri, S., Weijers, D., Lechner, E., Yamada, M.,
Hobbie, L. et al. (2005a) Plant development is regulated by a
family of auxin receptor F box proteins. Dev. Cell 9: 109–119.
Dharmasiri, S. and Estelle, M. (2002) The role of regulated protein
degradation in auxin response. Plant Mol. Biol. 49: 401–409.
Dhonukshe, P., Weits, D.A., Cruz-Ramirez, A., Deinum, E.E.,
Tindemans, S.H., Kakar, K. et al. (2012) A PLETHORA–auxin transcription module controls cell division plane rotation through
MAP65 and CLASP. Cell 149: 383–396.
Dhonukshe, P., Tanaka, H., Goh, T., Ebine, K., Mähönen, A.P.,
Prasad, K. et al. (2008) Generation of cell polarity in plants
links endocytosis, auxin distribution and cell fate decisions.
Nature 456: 962–966.
Dhonukshe, P. and Gadella, T.W. Jr (2003) Alteration of microtubule
dynamic instability during preprophase band formation revealed by
yellow fluorescent protein–CLIP170 microtubule plus-end labeling.
Plant Cell 15: 597–611.
Di Laurenzio, L., Wysocka-Diller, J., Malamy, J.E., Pysh, L., Helariutta, Y.,
Freshour, G. et al. (1996) The SCARECROW gene regulates an
asymmetric cell division that is essential for generating the radial
organization of the Arabidopsis root. Cell 86: 423–433.
DiDonato, R.J., Arbuckle, E., Buker, S., Sheets, J., Tobar, J., Totong, R.
et al. (2004) Arabidopsis ALF4 encodes a nuclear-localized protein
required for lateral root formation. Plant J. 37: 340–353.
Dolan, L., Janmaat, K., Willemsen, V., Linstead, P., Poethig, S.,
Roberts, K. et al. (1993) Cellular organisation of the Arabidopsis
thaliana root. Development 119: 71–84.
Dubrovsky, J.G., Sauer, M., Napsucialy-Mendivil, S., Ivanchenko, M.G.,
Friml, J., Shishkova, S. et al. (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc. Natl Acad.
Sci. USA 105: 8790–8794.
Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T. et al.
(2003) Efflux-dependent auxin gradients establish the apical–basal
axis of Arabidopsis. Nature 426: 147–153.
Fukaki, H., Nakao, Y., Okushima, Y., Theologis, A. and Tasaka, M.
(2005) Tissue-specific expression of stabilized SOLITARY-ROOT/
IAA14 alters lateral root development in Arabidopsis. Plant J. 44:
3823–95.
Fukaki, H., Tameda, S., Masuda, H. and Tasaka, M. (2002) Lateral root
formation is blocked by a gain-of-function mutation in the
SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J. 29: 153–168.
340
Furutani, M., Vernoux, T., Traas, J., Kato, T., Tasaka, M. and Aida, M.
(2004) PIN-FORMED1 and PINOID regulate boundary formation
and cotyledon development in Arabidopsis embryogenesis.
Development 131: 5021–5030.
Gagne, J.M. and Clark, S.E. (2010) The Arabidopsis stem cell factor
POLTERGEIST is membrane localized and phospholipid stimulated.
Plant Cell 22: 729–743.
Gagne, J.M., Song, S.K. and Clark, S.E. (2008) POLTERGEIST and PLL1
are required for stem cell function with potential roles in cell
asymmetry and auxin signaling. Commun. Integr. Biol. 1: 53–55.
Galinha, C., Hofhuis, H., Luijten, M., Willemsen, V., Blilou, I., Heidstra, R.
et al. (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449: 1053–1057.
Gallagher, K.L., Paquette, A.J., Nakajima, K. and Benfey, P.N. (2004)
Mechanisms regulating SHORT-ROOT intercellular movement.
Curr. Biol. 14: 1847–1851.
Geldner, N., Richter, S., Vieten, A., Marquardt, S., Torres-Ruiz, R.A.,
Mayer, U. et al. (2004) Partial loss-of-function alleles reveal a role
for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development 131: 389–400.
Gong, Y., Mo, C. and Fraser, S.E. (2004) Planar cell polarity signalling
controls cell division orientation during zebrafish gastrulation.
Nature 430: 689–693.
Guilfoyle, T.J. and Hagen, G. (2007) Auxin response factors. Curr. Opin.
Plant Biol. 10: 453–460.
Gunning, B.E.S., Hughes, J.E. and Hardham, A.R. (1978) Formative and
proliferative cell divisions, cell differentiation, and developmental
changes in the meristem of Azolla roots. Planta 143: 121–144.
Haecker, A., Gross-Hardt, R., Geiges, B., Sarkar, A., Breuninger, H.,
Herrmann, M. et al. (2004) Expression dynamics of WOX genes
mark cell fate decisions during early embryonic patterning in
Arabidopsis thaliana. Development 131: 657–668.
Hardtke, C.S. and Berleth, T. (1998) The Arabidopsis gene
MONOPTEROS encodes a transcription factor mediating embryo
axis formation and vascular development. EMBO J. 17: 1405–1411.
Hamann, T., Benková, E., Bäurle, I., Kientz, M. and Jürgens, G. (2002)
The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes
Dev. 16: 1610–1615.
Hamann, T., Mayer, U. and Jürgens, G. (1999) The auxin-insensitive
bodenlos mutation affects primary root formation and apical–basal
patterning in the Arabidopsis embryo. Development 126:
1387–1395.
Heidstra, R., Welch, D. and Scheres, B. (2004) Mosaic analyses using
marked activation and deletion clones dissect Arabidopsis
SCARECROW action in asymmetric cell division. Genes Dev. 18:
1964–1969.
Helariutta, Y., Fukaki, H., Wysocka-Diller, J., Nakajima, K., Jung, J.,
Sena, G. et al. (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:
555–567.
Hoshino, H., Yoneda, A., Kumagai, F. and Hasezawa, S. (2003) Roles
of actin-depleted zone and preprophase band in determining the
division site of higher-plant cells. Protoplasma 222: 157–165.
Jeong, S., Bayer, M. and Lukowitz, W. (2011) Taking the very first steps:
from polarity to axial domains in the early Arabidopsis embryo.
J. Exp. Bot. 62: 1687–1697.
Jürgens, G., Grebe, M. and Steinmann, T. (1997) Establishment of cell
polarity during early plant development. Curr. Opin. Cell Biol. 9:
849–852.
Plant Cell Physiol. 54(3): 333–342 (2013) doi:10.1093/pcp/pcs175 ! The Author 2012.
Formative cell divisions
Jürgens, G., Mayer, U., Busch, M., Lukowitz, W. and Laux, T. (1995)
Pattern formation in the Arabidopsis embryo: a genetic perspective.
Philos. Trans. R. Soc. B: Biol. Sci. 350: 19–25.
Jürgens, G., Mayer, U., Torres-Ruiz, R.A., Berleth, T. and Misera, S.
(1991) Genetic analysis of pattern formation in the Arabidopsis
embryo. Development 113: 27–38.
Kirik, V., Herrmann, U., Parupalli, C., Sedbrook, J.C., Ehrhardt, D.W. and
Hülskamp, M. (2007) CLASP localizes in two discrete patterns
on cortical microtubules and is required for cell morphogenesis
and cell division in Arabidopsis. J. Cell Sci. 120: 4416–4425.
Kleine-Vehn, J., Huang, F., Naramoto, S., Zhang, J., Michniewicz, M.,
Offringa, R. et al. (2009) PIN auxin efflux carrier polarity is regulated
by PINOID kinase-mediated recruitment into GNOM-independent
trafficking in Arabidopsis. Plant Cell 21: 3839–3849.
Kleine-Vehn, J., Langowski, L., Wisniewska, J., Dhonukshe, P.,
Brewer, P.B. and Friml, J. (2008) Cellular and molecular requirements for polar PIN targeting and transcytosis in plants.
Mol. Plant 1: 1056–1066.
Knoblich, J.A. (2010) Asymmetric cell division: recent developments
and their implications for tumour biology. Nat. Rev. Mol. Cell. Biol.
11: 849–860.
Laskowski, M.J., Williams, M.E., Nusbaum, H.C. and Sussex, I.M. (1995)
Formation of lateral root meristems is a two-stage process.
Development 121: 3303–3310.
Lokerse, A.S. and Weijers, D. (2009) Auxin enters the matrix assembly
of response machineries for specific outputs. Curr. Opin. Plant Biol.
12: 520–526.
Lucas, M., Guedon, Y., Jay-Allemand, C., Godin, C. and Laplaze, L.
(2008) An auxin transport-based model of root branching in
Arabidopsis thaliana. PLoS One 3: e3673.
Mayer, U., Büttner, G. and Jürgens, G. (1993) Apical–basal pattern
formation in the Arabidopsis embryo: studies on the role of the
gnom gene. Development 117: 149–162.
Mayer, U., Torres Ruiz, R.A., Berleth, T., Miséra, S. and Jürgens, G.
(1991) Mutations affecting body organization in the Arabidopsis
embryo. Nature 353: 402–407.
Mollinari, C., Kleman, J.P., Jiang, W., Schoehn, G., Hunter, T. and
Margolis, R.L. (2002) PRC1 is a microtubule binding and bundling
protein essential to maintain the mitotic spindle midzone. J. Cell
Biol. 157: 1175–1186.
Moreno-Risueno, M.A., Van Norman, J.M., Moreno, A., Zhang, J.,
Ahnert, S.E. and Benfey, P.N. (2010) Oscillating gene expression
determines competence for periodic Arabidopsis root branching.
Science 329: 1306–1311.
Müller, S., Han, S. and Smith, L.G. (2006) Two kinesins are involved in
the spatial control of cytokinesis in Arabidopsis thaliana. Curr. Biol.
16: 888–894.
Müller, S., Wright, A.J. and Smith, L.G. (2009) Division plane control in
plants: new players in the band. Trends Cell Biol. 19: 180–188.
Nawy, T., Bayer, M., Mravec, J., Friml, J., Birnbaum, K.D. and
Lukowitz, W. (2010) The GATA factor HANABA TARANU is
required to position the proembryo boundary in the early
Arabidopsis embryo. Dev. Cell 19: 103–113.
Nogami, A. and Mineyuki, Y. (1999) Loosening of a preprophase band
of microtubules in onion (Allium cepa L.) root tip cells by kinase
inhibitors. Cell Struct. Funct. 24: 419–424.
Okushima, Y., Fukaki, H., Onoda, M., Theologis, A. and Tasaka, M.
(2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19:
118–130.
Okushima, Y., Overvoorde, P.J., Arima, K., Alonso, J.M., Chan, A.,
Chang, C. et al. (2005) Functional genomic analysis of the AUXIN
RESPONSE FACTOR gene family members in Arabidopsis thaliana:
unique and overlapping functions of ARF7 and ARF19. Plant Cell 17:
444–463.
Paponov, I.A., Teale, W.D., Trebar, M., Blilou, I. and Palme, K. (2005)
The PIN auxin efflux facilitators: evolutionary and functional perspectives. Trends Plant Sci. 10: 170–177.
Péret, B., De Rybel, B., Casimiro, I., Benková, E., Swarup, R., Laplaze, L.
et al. (2009) Arabidopsis lateral root development: an emerging
story. Trends Plant Sci. 14: 399–408.
Peris, C.I., Rademacher, E.H. and Weijers, D. (2010) Green beginnings—
pattern formation in the early plant embryo. Curr. Top. Dev. Biol. 91:
1–27.
Pickett-Heaps, J.D. and Northcote, D.H. (1966) Organization of microtubules and endoplasmic reticulum during mitosis and cytokinesis
in wheat meristems. J. Cell Sci. 1: 109–120.
Quesada-Hernández, E., Caneparo, L., Schneider, S., Winkler, S.,
Liebling, M., Fraser, S.E. et al. (2010) Stereotypical cell division
orientation controls neural rod midline formation in zebrafish.
Curr. Biol. 20: 1966–1972.
Rasmussen, C.G., Humphries, J.A. and Smith, L.G. (2011a)
Determination of symmetric and asymmetric division planes in
plant cells. Annu. Rev. Plant Biol. 62: 387–409.
Rasmussen, C.G., Sun, B. and Smith, L.G. (2011b) Tangled localization
at the cortical division site of plant cells occurs by several mechanisms. J. Cell Sci. 124: 270–279.
Reinhardt, D., Mandel, T. and Kuhlemeier, C. (2000) Auxin regulates
the initiation and radial position of plant lateral organs. Plant Cell
12: 507–518.
Robert, H.S. and Offringa, R. (2008) Regulation of auxin transport
polarity by AGC kinases. Curr. Opin. Plant Biol. 11: 495–502.
Rouse, D., Mackay, P., Stirnberg, P., Estelle, M. and Leyser, O. (1998)
Changes in auxin response from mutations in an AUX/IAA gene.
Science 279: 1371–1373.
Sabatini, S., Heidstra, R., Wildwater, M. and Scheres, B. (2003)
SCARECROW is involved in positioning the stem cell niche in the
Arabidopsis root meristem. Genes Dev. 17: 354–358.
Sarkar, A.K., Luijten, M., Miyashima, S., Lenhard, M., Hashimoto, T.,
Nakajima, K. et al. (2007) Conserved factors regulate signalling in
Arabidopsis thaliana shoot and root stem cell organizers. Nature
446: 811–814.
Sasabe, M., Kosetsu, K., Hidaka, M., Murase, A. and Machida, Y. (2011)
Arabidopsis thaliana MAP65-1 and MAP65-2 function redundantly
with MAP65-3/PLEIADE in cytokinesis downstream of MPK4. Plant
Signal. Behav. 6: 743–747.
Sasabe, M., Soyano, T., Takahashi, Y., Sonobe, S., Igarashi, H. and
Itoh, T.J. (2006) Phosphorylation of NtMAP65-1 by a MAP kinase
down-regulates its activity of microtubule bundling and stimulates
progression of cytokinesis of tobacco cells. Genes Dev. 20:
1004–1014.
Scheres, B. and Benfey, P.N. (1999) Asymmetric cell division in plants.
Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 505–537.
Scheres, B., Di Laurenzio, L., Willemsen, V., Hauser, M.T., Janmaat, K.,
Weisbeek, P. et al. (1995) Mutations affecting the radial organisation of the Arabidopsis root display specific defects throughout the
radial axis. Development 121: 53–62.
Schlereth, A., Moller, B., Liu, W., Kientz, M., Flipse, J., Rademacher, E.H.
et al. (2010) MONOPTEROS controls embryonic root initiation by
regulating a mobile transcription factor. Nature 464: 913–916.
Plant Cell Physiol. 54(3): 333–342 (2013) doi:10.1093/pcp/pcs175 ! The Author 2012.
341
M. Smolarkiewicz and P. Dhonukshe
Siller, K.H. and Doe, C.Q. (2009) Spindle orientation during asymmetric cell division. Nat. Cell Biol. 11: 365–374.
Smertenko, A.P., Chang, H.Y., Wagner, V., Kaloriti, D., Fenyk, S.,
Sonobe, S. et al. (2004) The Arabidopsis microtubule-associated
protein AtMAP65-1: molecular analysis of its microtubule bundling
activity. Plant Cell 16: 2035–2047.
Smith, L.G. (2001) Plant cell division: building walls in the right places.
Nat. Rev. Mol. Cell. Biol. 2: 33–39.
Song, S.K., Hofhuis, H., Lee, M.M. and Clark, S.E. (2008) Key divisions in
the early Arabidopsis embryo require POL and PLL1 phosphatases
to establish the root stem cell organizer and vascular axis. Dev. Cell
15: 98–109.
Song, S.K., Lee, M.M. and Clark, S.E. (2006) POL and PLL1 phosphatases
are CLAVATA1 signaling intermediates required for Arabidopsis
shoot and floral stem cells. Development 133: 4691–4698.
Song, S.K. and Clark, S.E. (2005) POL and related phosphatases
are dosage-sensitive regulators of meristem and organ development
in Arabidopsis. Dev. Biol. 285: 272–284.
Sorefan, K., Girin, T., Liljegren, S.J., Ljung, K., Robles, P., GalvánAmpudia, C.S. et al. (2009) A regulated auxin minimum is required
for seed dispersal in Arabidopsis. Nature 459: 583–586.
Sozzani, R., Cui, H., Moreno-Risueno, M.A., Busch, W., Van
Norman, J.M., Vernoux, T. et al. (2010) Spatiotemporal regulation
of cell-cycle genes by SHORTROOT links patterning and growth.
Nature 466: 128–132.
Torres-Ruiz, R.A. and Jürgens, G. (1994) Mutations in the FASS gene
uncouple pattern formation and morphogenesis in Arabidopsis
development. Development 120: 2967–2978.
Traas, J., Bellini, C., Nacry, P., Kronenberger, J., Bouchez, D. and
Caboche, M. (1995) Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375: 676–677.
Ulmasov, T., Hagen, G. and Guilfoyle, T.J. (1999) Activation and
repression of transcription by auxin-response factors. Proc. Natl
Acad. Sci. USA 96: 5844–5849.
342
Van Damme, D., De Rybel, B., Gudesblat, G., Demidov, D.,
Grunewald, W., De Smet, I. et al. (2011) Arabidopsis a Aurora
kinases function in formative cell division plane orientation. Plant
Cell 23: 4013–4024.
Van Damme, D. (2009) Division plane determination during plant
somatic cytokinesis. Curr. Opin. Plant Biol. 12: 745–751.
Vanstraelen, M., Van Damme, D., De Rycke, R., Mylle, E., Inzé, D. and
Geelen, D. (2006) Cell cycle-dependent targeting of a kinesin at
the plasma membrane demarcates the division site in plant cells.
Curr. Biol. 16: 308–314.
Walker, K.L., Muller, S., Moss, D., Ehrhardt, D.W. and Smith, L.G. (2007)
Arabidopsis TANGLED identifies the division plane throughout
mitosis and cytokinesis. Curr. Biol. 17: 1827–1836.
Weijers, D., Benkova, E., Jäger, K.E., Schlereth, A., Hamann, T., Kientz, M.
et al. (2005) Developmental specificity of auxin response by pairs
of ARF and Aux/IAA transcriptional regulators. EMBO J. 24:
1874–1885.
Weijers, D., Schlereth, A., Ehrismann, J.S., Schwank, G., Kientz, M. and
Jürgens, G. (2006) Auxin triggers transient local signaling for cell
specification in Arabidopsis embryogenesis. Dev. Cell 10: 265–270.
Wildwater, M., Campilho, A., Perez-Perez, J.M., Heidstra, R., Blilou, I.
and Korthout, H. (2005) The RETINOBLASTOMA-RELATED gene
regulates stem cell maintenance in Arabidopsis roots. Cell 123:
1337–1349.
Worley, C.K., Zenser, N., Ramos, J., Rouse, D., Leyser, O., Theologis, A.
et al. (2000) Degradation of Aux/IAA proteins is essential for
normal auxin signalling. Plant J. 21: 553–562.
Wright, A.J., Gallagher, K. and Smith, L.G. (2009) discordia1 and alternative discordia1 function redundantly at the cortical division site
to promote preprophase band formation and orient division planes
in maize. Plant Cell 21: 234–247.
Wu, X., Chory, J. and Weigel, D. (2007) Combinations of WOX activities regulate tissue proliferation during Arabidopsis embryonic
development. Dev. Biol. 309: 306–316.
Plant Cell Physiol. 54(3): 333–342 (2013) doi:10.1093/pcp/pcs175 ! The Author 2012.