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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.