Prenatal Plumbing – Vascular Tissue Formation in the Plant Embryo Bert De Rybel∗, Alice S

Home , Embryo

MINIREVIEW Prenatal plumbing – vascular tissue formation in the plant embryo Bert De Rybel∗, Alice S. Breda and Dolf Weijers∗

Laboratory of Biochemistry, Wageningen University, Wageningen, 6703HA, the Netherlands

Correspondence The first vascular tissue precursors are specified early during embryogenesis. *Corresponding authors, These precursors give rise to the multi-layered cylinder of hypocotyl e-mail: [email protected]; and root through controlled, oriented divisions. Concomitant with its [email protected] growth, the bundle is patterned into xylem and phloem tissues, and Received 3 May 2013; intervening procambial cells. These patterns are later maintained during post- revised 1 July 2013 embryonic growth and vascular cells will eventually differentiate, displaying characteristic secondary cell wall modifications. Given that the vascular doi:10.1111/ppl.12091 system forms de novo in a simple yet predictable fashion, the embryo provides an excellent model system to study early developmental aspects of vascular tissue formation. However, the benefits of this model are only beginning to be exploited, and most knowledge about the vascular development is derived from growing post-embryonic tissues. Importantly, it is unclear how much of these established post-embryonic mechanisms can be extrapolated to tissue formation during embryogenesis. Here we review concepts established in the model plant Arabidopsis thaliana and focus on recent advances made in understanding embryonic vascular development.

Introduction and intervening cambium cells. Post-embryonically, these tissues will differentiate into anatomically recog- The evolution of an efficient fluid conducting system, nizable structures by secondary cell wall thickenings, consisting of xylem and phloem tissues allowed plants to characteristic for both xylem and phloem tissues. Our grow beyond the size of mosses like Physcomitrella and understanding of post-embryonic vascular development, reach the size of vascular trees we know today (Raven tissue maintenance and differentiation has increased et al. 1999). The plant vascular system is vital to transport tremendously in the past years (Ohashi-Ito and Fukuda water, sugars and nutrients throughout the plant. During 2010, Scarpella and Helariutta 2010, Miyashima et al. early embryogenesis, vascular tissues are first specified 2013b). Nevertheless, as vascular tissues are specified from a limited number of provascular initial cells, and first patterned before germination, these develop- four in the model plant Arabidopsis thaliana (Scheres mental aspects are best studied during embryogenesis. et al. 1994). Next, the tissue is established by oriented Here, we will describe the current knowledge and recent cell divisions and finally the vascular bundle will be advances made in understanding embryonic vascular patterned into distinct zones including xylem, phloem tissue specification, establishment and patterning and

Abbreviations – AHP6, ARABIDOPSIS HISTIDINE PHOSPHOTRANSFER PROTEIN6; APL, ALTERED PHLOEM DEVELOPMENT; ARF5/MP, AUXIN RESPONSE FACTOR5/MONOPTEROS; bHLH, basic helix-loop-helix; BRX, BREVIS RADIX; CNA, CORONA; HD-ZIPIII, class III homeo-domain leucine zipper; HLH, helix-loop-helix; IFL1/REV, INTERFASICULAR FIBRELESS1/REVOLUTA; OPS, OCTOPUS; PHB, PHABULOSA; PHV, PHAVOLUTA; PIN7, PIN-FORMED7; PLL1, POLTERGEIST LIKE1; POL, POLTERGEIST; RLKs, receptor-like kinases; RPK1, RECEPTOR-LIKE PROTEIN KINASE1; SCR, SCARECROW; SHR, SHORTROOT; TOAD2, TOADSTOOL2.

126 Physiol. Plant. 151, 2014 highlight future challenges. We will discuss the major form the shoot tissues (Emery et al. 2003, Miyashima events and key players involved in these developmental et al. 2013a). In the post-embryonic root, all five processes in a chronological order, and focus on closely related HD-ZIPIII class transcription factors findings in Arabidopsis. PHB, PHV, REV, ATHB8 and ATHB15/CORONA (CNA) (Talbert et al. 1995, Baima et al. 2001, McConnell et al. 2001, Green et al. 2005, Prigge et al. 2005) Early patterning events are expressed in overlapping patterns within the stele. After fertilization of the egg cell, the zygote undergoes The SHORTROOT (SHR) – SCARECROW (SCR) pathway an asymmetric anticlinal (within the cell file) division to activates miR165/6 in the endodermis (Carlsbecker et al. form a small upper cell and a larger basal cell (1-cell 2010). These miRNA’s are able to move into the stage, Fig. 1) (Scheres et al. 1994). Asymmetric local- vascular bundle, where they can degrade the HD-ZIPIII ization of the auxin efflux transporters PIN-FORMED7 transcripts. The higher levels of miR165/6 close to the (PIN7) protein ensures that an auxin maximum is estab- endodermis and lower in the center of the stele create lished in the upper cell. Next, the upper cell divides per- a gradient of HD-ZIPIII transcripts. It was suggested that iclinally (creating an additional cell file). An additional this differential dosage along the xylem axis of the root anticlinal division generates the octant stage embryo defines proto- or metaxylem identity (Carlsbecker et al. (Fig. 1) and each of the eight cells undergoes an oblique 2010). Besides the early embryonic expression of PHB, division that separates the protoderm from the inner it was recently shown that at least five of the miRNAs tissues (dermatogen stage, Fig. 1) (Scheres et al. 1994). in the miR165/6 family are expressed in the lower tier Evidently, the correct progression of these ‘pre- of early stage embryos, restricting PHB expression to vascular’ stages is critical to ensure that vascular the upper tier during this stage of development (Figs development starts from the right number of cells, and 1 and 2) (Miyashima et al. 2013a). Nevertheless, as in the right position. Several of the genes that act later PHB, PHV and REV expression in the embryonic root during (post-embryonic) vascular patterning are already is only first seen around late heart to torpedo stage expressed at the earliest stages of embryogenesis. For (Emery et al. 2003, Williams et al. 2005, Smith and Long example, the transcription factors AUXIN RESPONSE 2010, Miyashima et al. 2013a), it is more likely that this FACTOR5/MONOPTEROS (ARF5/MP) (Hamann et al. early shoot expression is more linked to its function in 2002) and its transcriptional repressor Aux/IAA controlling ab- and adaxial polarity (Prigge et al. 2005) PROTEIN12/BODENLOS (IAA12/BDL, Figs 1 and 2) than to vascular patterning. (Hamann et al. 2002) are already expressed in the first In conclusion, several components of vascular tissue apical cell. At later stages, mp and bdl mutants show patterning are expressed in embryos at stages prior to strong vascular defects in the cotyledons, have a strongly vascular tissue formation. An interesting, yet unanswered reduced number of vascular cells in the hypocotyl and question therefore is whether the early embryo is perhaps fail to establish a root altogether (Berleth and Jurgens poised for rapid and efficient vascular tissue initiation. 1993, Hardtke and Berleth 1998, Hamann et al. 1999, 2002). Besides these auxin signaling components, the Establishment of vascular tissues disruption of any other factor involved in the tightly controlled processes of auxin biosynthesis (e.g. YUCCA, The combined action of auxin efflux carriers PIN1 and SHI/STY), PIN-dependent transport (e.g. GNOM) or cell PIN7 will focus the auxin maximum to the top suspensor divisions (e.g. FACKEL), will lead to aberrantly formed cell when embryos enter the globular stage (Figs 1 embryos (Steinmann et al. 1999, Schrick et al. 2000, and 2) (Friml et al. 2003). Together with the mobile Cheng et al. 2007, Baylis et al. 2012). It is thus clear helix-loop-helix (HLH) transcription factor TARGET OF that auxin activity is critical for the formation of vascular MONOPTEROS7 (TMO7/bHLH135/ATBS1) that moves tissue, but it remains to be demonstrated whether the from the MP expression domain to the uppermost very early activity of these response components is suspensor cell, auxin will specify this cell to become causally related. the hypophysis, the future organizer of the root stem A second category of factors whose later activity cell niche (Weijers et al. 2006, Schlereth et al. 2010). in vascular tissue is evident, and whose expression The globular stage is further marked by the periclinal commences early during embryogenesis are the class III divisions of the inner cells and at this stage, all three homeo-domain leucine zipper (HD-ZIPIII) transcription major plant tissues, protoderm (later called epidermis), factors PHABULOSA (PHB), PHAVOLUTA (PHV) and ground tissue and vascular tissues are represented INTERFASICULAR FIBRELESS1/REVOLUTA (IFL1/REV). by a unique population of precursor cells (Fig. 1) All these genes are expressed in the upper tier that will (Scheres et al. 1994). At this early globular stage,

Physiol. Plant. 151, 2014 127 Fig. 1. Schematic representation of embryo development in Arabidopsis thaliana. Longitudinal sections are shown on top and corresponding transverse cross sections (taken at the indicated gray dotted line) at the bottom. The timing of the first expression of each of the key players in vascular development is indicated in the developmental axis (cot.: cotelydon). the anatomical delineation of the four inner cells as both families of bHLH transcription factors are able vascular precursor cells logically coincides with the to form heterodimer complexes in vitro (Ohashi-Ito and expression of the first vascular specific markers. Although Bergmann 2007) and in planta (De Rybel et al. 2013). the actual specification event itself, generating the Higher order tmo5 (De Rybel et al. 2013) or lhw (De provascular initial cells, remains elusive to date, some Rybel et al. 2013, Ohashi-Ito et al. 2013a) mutants show key players of vascular tissue formation in the embryo a strongly reduced number of vascular periclinal cell have been described recently. As mentioned before, divisions during embryogenesis and post-embryonically. MP controls many aspects of embryo development The domain of predicted TMO5-LHW dimer formation, besides hypophysis specification, including vascular defined by the overlap of the two gene expression development (Berleth and Jurgens 1993, Hardtke and domains, is confined to provascular cells in globular Berleth 1998). One of its direct target genes, the basic stage embryos and becomes restricted to the young helix-loop-helix (bHLH) transcription factor TARGET xylem cells later in development (Fig. 2). Intriguingly, OF MONOPTEROS5 (TMO5/bHLH32) was identified combined misexpression of TMO5 and LHW specifically as a good candidate for this function because it is induces periclinal cell divisions in any cell type. These expressed in the provascular initial cells at early globular data suggest that the TMO5-LHW dimer is required and stage embryos (Figs 1 and 2) (Schlereth et al. 2010). sufficient to control the periclinal divisions involved Although single tmo5 mutants do not show phenotypes, in the establishment of the vascular tissue during the tmo5 tmo5-like1 double mutant shows a strongly embryogenesis and for maintenance of the vasculature reduced vascular bundle with monarch symmetry (De in a growing post-embryonic root (De Rybel et al. 2013). Rybel et al. 2013), identical to the lonesome highway Besides the role of these bHLH transcription factors (lhw/bhlh156) mutant (Ohashi-Ito and Bergmann 2007). in controlling periclinal divisions in the vasculature, TMO5 and LHW each have several homologs and the phosphatases POLTERGEIST (POL) and the related

128 Physiol. Plant. 151, 2014 POLTERGEIST LIKE1 (PLL1) are required for key asymmetric divisions generating the vasculature and stem cell regions (Song et al. 2008). Although single mutants show no phenotype, the pol pll1 double mutant displays symmetric divisions in the provascular initial cells compared to the asymmetric division in wild type from early to late globular stage (Fig. 1) (Song et al. 2008). As a conse- quence, the pol pll1 mutants lack expression of vascular markers, indicating a loss of vascular identity and post- embryonically they lack vascular tissues all together (Song et al. 2008). Also, two receptor-like kinases (RLKs) are required for proper cambial establishment: RECEPTOR-LIKE PROTEIN KINASE1 (RPK1) and TOAD- STOOL2 (TOAD2) first expressed at octant and globular stage, respectively (Figs 1 and 2) (Nodine et al. 2007). Loss of these redundantly acting RLKs causes ectopic expression of provascular markers in the protoderm and these rpk1 toad2 double mutants fail to establish the major tissue types, suggesting aberrant radial patterning of these early embryos (Nodine et al. 2007). Although these phosphatases and kinases are clearly crucial for proper vascular development during embryogenesis, they have not been linked to other existing pathways so far. It will be interesting to see whether these kinases and phosphatases operate in the same pathway, and how this connects to other known components such as the previously mentioned MP-TMO5/LHW pathway. Importantly, especially the POL and PLL phosphatases appear to act very early in vascular tissue formation, based on defective cell divisions. As no early markers were analyzed, it remains to be seen whether they indeed control initiation of vascular cell fate. One of the first vascular mutants identified, wooden leg (wol), shows a strong reduction in the number of post-embryonic provascular cell files, which all have acquired a protoxylem identity (Scheres et al. 1995). WOL/CRE1/AHK4 encodes a two-component histidine kinase protein that together with AHK2 and AHK3 represents the known cytokinin receptors (Mah¨ onen¨ et al. 2000, 2006b, Bishopp et al. 2009). Although WOL is expressed in provascular cells from the late globular stage onwards, phenotypes in the wol allele of CRE1/AHK4, or in the cre1 ahk2 ahk3 triple loss- of-function mutant have only been described post- embryonically (Mah¨ onen¨ et al. 2000, 2006b). Neverthe- less, the expression during late globular stage suggests a function of cytokinin signaling during embryogenesis. Fig. 2. Overview of expression patterns of key regulators of vascular Further down in the cytokinin-signaling cascade, ARA- development during embryo development in Arabidopsis.RPK1and BIDOPSIS HISTIDINE PHOSPHOTRANSFER PROTEIN6 TOAD2 overlap in the central domain protoderm. Note that suspensor expression after globular stage is not clear from literature and has (AHP6) lacks a conserved histidine residue required been omitted. Also, note that APL and OPS are not yet expressed at for phosphotransfer activity and hence acts as an the indicated stages, but expression is first seen around late heart to inhibitor of signaling (Mah¨ onen¨ et al. 2006a). AHP6 torpedo stage. is expressed specifically at the protoxylem poles of the

Physiol. Plant. 151, 2014 129 post-embryonic root, although the protein appears to be hypocotyl, while strong root specific expression is only more broadly expressed and ahp6 mutants only show clear post-embryonically for most (Fig. 2) (Bonke et al. sporadic loss of differentiated protoxylem (Mah¨ onen¨ 2003, Bauby et al. 2007, Truernit et al. 2012). et al. 2006a). At late globular stage, AHP6 is expressed in the future cotyledon tips (Figs 1 and 2) (Bishopp Back to the future et al. 2011), suggesting that at least the future shoot has adopted a bilateral symmetry, at a stage where the The initial specification and establishment of vascular root still appears radially symmetric with uniform TMO5 tissues takes place in the early embryo, but no vascular expression in all provascular cells (De Rybel et al. 2013). differentiation (typed by secondary cell wall thickenings) Whether cytokinin signaling controls early events during can be seen until after germination (Fig. 3). As none of the vascular tissue patterning in the embryo, and how its differentiation genes is expressed before the late heart to activity is connected to other components of vascular torpedo stage (Fig. 2), the embryo represents an excellent tissue formation remains to be determined. model system to study vascular specification and establishment. Moreover, it will be crucial to study patterning in the early embryo, as the pattern established during Late specification events embryogenesis is mostly maintained post-embryonically Around the transition stage, the four provascular cell during growth. As most studies on vascular development files divide periclinally, delineating the pericycle (Fig. 1). were conducted in post-embryonic tissues, and often At the same time, the ground tissue initial cells undergo use terminal differentiation markers (such as cell wall their first asymmetric divisions to form cortex and endo- patterns) to assess patterns, direct knowledge on earlier dermal layers (Fig. 1) (Scheres et al. 1994). At the heart steps is limited. In this section we consider important stage, further periclinal divisions increase the number patterning mechanisms that have surfaced in studies on of vascular cell files. Following the establishment of later stages, and we discuss if and how these may apply the cortex and endodermis, PHB expression extends to early embryogenesis. from the cotyledon tips into the root (Emery et al. 2003, One of the most intriguing aspects of early vascular Miyashima et al. 2013a). Also AHP6 extends into the tissue formation is that xylem-specific genes appear to be root in two strands, suggesting protoxylem identity is expressed earlier than phloem specific genes (Figs 1 and established at this point (Mah¨ onen¨ et al. 2006a). Addi- 2). Although it is possible that early phloem specification tionally, at this stage, TMO5 adopts its xylem-specific genes have not been identified so far, it is more likely that expression pattern (De Rybel et al. 2013), suggesting that xylem is specified before phloem during embryogenesis. symmetry breakage is now also established in the root. Interestingly, phloem mutants such as apl (Bonke et al. Around the late heart stage, phloem markers are first expressed. A key regulator of phloem identity is the MYB type transcription factor ALTERED PHLOEM DEVELOP- MENT (APL) (Bonke et al. 2003). Ectopic expression of APL is able to repress xylem development, while apl mutants show xylem like cells developing where phloem would normally form (Bonke et al. 2003). Moreover, apl mutants lack sieve elements and companion cells, suggesting APL both represses xylem differentiation and promotes phloem differentiation (Bonke et al. 2003). Several other phloem specific genes have been identified through screening gene-trap lines (Bauby et al. 2007). One of these, the polarly localized membrane protein OCTOPUS (OPS) also controls phloem differentiation (Truernit et al. 2012). Very similar phloem defects have been described in another of these gene-trap lines, which was previously identified as BREVIS RADIX (BRX) (Mouchel et al. 2006, Scacchi et al. 2010), which is itself Fig. 3. 3D reconstruction of confocal image stack of a mature a MP target gene (Scacchi et al. 2010) and shows low Arabidopsis embryo. The image shows the vascular cells in root, penetrance mp-like embryo phenotypes (Scacchi et al. hypocotyl and cotyledons and highlights the root apical meristem and 2009). Intriguingly, all of these genes are first expressed vascular strands in the cotyledons. Note the absence of differentiated in late heart to torpedo stage embryos in cotyledons and vascular tissues marked by secondary cell wall thickenings.

130 Physiol. Plant. 151, 2014 2003) and ops (Truernit et al. 2012), still show abnormal We have reviewed several recent concepts that have but differentiated xylem tissues, while mutants with loss emerged from studies on vascular tissue formation and of the xylem-specific TMO5 clade (tmo5 quadruple) do patterning in the embryo, and we have explored whether not show any vascular cells. These lines of evidence mechanisms that are known to operate later could also suggest that the xylem could act as an organizer for the work in the embryo. It should be evident that the vascular tissues (De Rybel et al. 2013). embryo offers excellent opportunities to dissect the most In a fully patterned post-embryonic root, auxin signal- elemental aspects of vascular tissue formation. As the ing is observed along the xylem axis, while cytokinin sig- very different cellular contexts of for example mature naling is strongest in the intervening procambium cells. root or leaf hamper direct translation of concepts to the This clear correlation led to the description of a mutually embryo, we advocate the use of the embryo itself as a inhibitory interaction between auxin and cytokinin (Bish- model. The recent development of methods to visualize opp et al. 2011). In this model, cytokinin promotes the the entire embryonic vascular tissue in 3D, as well as a PIN auxin efflux carriers to redirect auxin to the central set of mutants that affect this stage of development (De xylem axis. Here, high auxin induces AHP6 expression, Rybel et al. 2013) should be a good starting point for the negative regulator of cytokinin signaling (Bishopp future studies. et al. 2011). Although it is clear from this work that xylem and phloem development are tightly linked, up to date it Acknowledgements – The authors would like to thank Saiko is unclear how this would happen exactly. Moreover, the Yoshida for help with MORPHOGRAPHX software and Jos R. mutually inhibitory feedback loop between auxin and Wendrich for critical reading of the manuscript. Work on cytokinin works in an already patterned post-embryonic vascular development and embryogenesis in our group is root. It will be a future challenge to find out how this funded by the European Research Council (Starting Grant mechanism works early in embryogenesis when the dis- ‘CELLPATTERN’, Contract no. 281573 to D. W.), by the tinct xylem and phloem domains are not yet established. Netherlands Organization for Scientific Research (NWO; The interconnection of auxin and cytokinin pathways ALW-VIDI-864.06.012 and ALW-820.02.019 to D. W.) and in a bistable, mutually inhibitory loop shows that by a Marie Curie long term FP7 Intra-European Fellowship the components presently known to affect vascular (IEF-2009-252503) to B. D. R. The authors declare that they tissue patterning may act in larger networks. Indeed, have no competing financial interests. other connections are evident from work on the HD-ZIP transcription factor in leaf venation. It was References very convincingly shown that the HD-ZIPIII class transcription factor ATHB8 plays a major role in leaf Baima S, Nobili F, Sessa G, Lucchetti S, Ruberti I, Morelli vein patterning post-embryonically by specifying correct G (1995) The expression of the Athb-8 homeobox gene PIN expression and localization domains, thus leading is restricted to provascular cells in Arabidopsis thaliana. to the formation of narrow leaf veins (Mattsson et al. Development 121: 4171–4182 2003, Scarpella et al. 2006, Donner et al. 2009). Not Baima S, Possenti M, Matteucci A, Wisman E, Altamura only does ATHB8 direct PIN-dependent auxin transport MM, Ruberti I, Morelli G (2001) The Arabidopsis patterns, the gene itself is also a direct target of the ATHB-8 HD-zip protein acts as a auxin response transcription factor MP (Donner et al. differentiation-promoting transcription factor of the 2009). This positive feedback loop auxin-MP-ATHB8- vascular meristems. Plant Physiol 126: 643–655 Bauby H, Divol F, Truernit E, Grandjean O, Palauqui JC PIN1-auxin works to restrict the preprocambial cell (2007) Protophloem differentiation in early Arabidopsis specification in developing leafs. Although most likely thaliana development. Plant Cell Physiol 48: 97–109 expressed at earlier stages as well, the first ATHB8 Baylis T, Cierlik I, Sundberg E, Mattsson J (2012) SHORT expression was described around heart stage (Baima INTERNODES/STYLISH genes, regulators of auxin et al. 1995, Mattsson et al. 2003). However, since all biosynthesis, are involved in leaf vein development in other components in this loop are present and active Arabidopsis thaliana. New Phytol 197: 737–750 at early stages of embryogenesis, it is likely that the Berleth T, Jurgens G (1993) The role of the monopteros loop operates much earlier. This notion is supported gene in organising the basal body region of the by the finding that ATHB8 misexpression can partially Arabidopsis embryo. Development 118: 575–587 suppress the narrow root vascular bundle phenotype of Bishopp A, Help H, Helariutta Y (2009) Cytokinin the lhw mutant (Ohashi-Ito et al. 2013b). A key future signaling during root development. Int Rev Cell Mol Biol challenge will be to comprehensively understand these 276: 1–48 interconnected networks, and to learn how growth and Bishopp A, Help H, El-Showk S, Weijers D, Scheres B, patterning are linked. Friml J, Benkova E, Mahonen AP, Helariutta Y (2011) A

Physiol. Plant. 151, 2014 131 mutually inhibitory interaction between auxin and Mah¨ onen¨ AP, Bishopp A, Higuchi M, Nieminen KM, cytokinin specifies vascular pattern in roots. Curr Biol Kinoshita K, Tormakangas K, Ikeda Y, Oka A, Kakimoto 21: 917–926 T, Helariutta Y (2006a) Cytokinin signaling and its Bonke M, Thitamadee S, Mahonen AP, Hauser MT, inhibitor AHP6 regulate cell fate during vascular Helariutta Y (2003) APL regulates vascular tissue identity development. Science 311: 94–98 in Arabidopsis. Nature 426: 181–186 Mah¨ onen¨ AP, Higuchi M, Tormakangas K, Miyawaki K, Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Pischke MS, Sussman MR, Helariutta Y, Kakimoto T Zhou J, Lindgren O, Moreno-Risueno MA, Vaten A, (2006b) Cytokinins regulate a bidirectional Thitamadee S, Campilho A, Sebastian J, Bowman JL, phosphorelay network in Arabidopsis. Curr Biol 16: Helariutta Y, Benfey PN (2010) Cell signalling by 1116–1122 microRNA165/6 directs gene dose-dependent root cell Mattsson J, Ckurshumova W, Berleth T (2003) Auxin fate. Nature 465: 316–321 signaling in Arabidopsis leaf vascular development. Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the Plant Physiol 131: 1327–1339 YUCCA flavin monooxygenases is essential for McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton embryogenesis and leaf formation in Arabidopsis. Plant MK (2001) Role of PHABULOSA and PHAVOLUTA in Cell 19: 2430–2439 determining radial patterning in shoots. Nature 411: DeRybelB,Moller¨ B, Yoshida S, Grabowicz I, Barbier de 709–713 Reuille P, Boeren S, Smith RS, Borst JW, Weijers D Miyashima S, Honda M, Hashimoto K, Tatematsu K, (2013) A bHLH complex controls embryonic vascular Hashimoto T, Sato-Nara K, Okada K, Nakajima K tissue establishment and indeterminate growth in (2013a) A comprehensive expression analysis of the Arabidopsis. Dev Cell 24: 426–437 Arabidopsis MICRORNA165/6 gene family during embryogenesis reveals a conserved role in meristem Donner TJ, Sherr I, Scarpella E (2009) Regulation of specification and a non-cell-autonomous function. Plant preprocambial cell state acquisition by auxin signaling Cell Physiol 54: 375–384 in Arabidopsis leaves. Development 136: 3235–3246 Miyashima S, Sebastian J, Lee JY, Helariutta Y (2013b) Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki Stem cell function during plant vascular development. A, Baum SF, Bowman JL (2003) Radial patterning of EMBO J 32: 178–193 Arabidopsis shoots by class III HD-ZIP and KANADI Mouchel CF, Osmont KS, Hardtke CS (2006) BRX mediates genes. Curr Biol 13: 1768–1774 feedback between brassinosteroid levels and auxin Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, signalling in root growth. Nature 443: 458–461 Hamann T, Offringa R, Jurgens¨ G (2003) Nodine MD, Yadegari R, Tax FE (2007) RPK1 and TOAD2 Efflux-dependent auxin gradients establish the are two receptor-like kinases redundantly required for apical-basal axis of Arabidopsis. Nature 426: 147–153 arabidopsis embryonic pattern formation. Dev Cell 12: Green KA, Prigge MJ, Katzman RB, Clark SE (2005) 943–956 CORONA, a member of the class III homeodomain Ohashi-Ito K, Bergmann DC (2007) Regulation of the leucine zipper gene family in Arabidopsis, regulates Arabidopsis root vascular initial population by stem cell specification and organogenesis. Plant Cell 17: LONESOME HIGHWAY. Development 134: 691–704 2959–2968 Hamann T, Mayer U, Jurgens G (1999) The Ohashi-Ito K, Fukuda H (2010) Transcriptional regulation auxin-insensitive bodenlos mutation affects primary root of vascular cell fates. Curr Opin Plant Biol 13: 670–676 formation and apical-basal patterning in the Arabidopsis Ohashi-Ito K, Matsukawa M, Fukuda H (2013a) An embryo. Development 126: 1387–1395 atypical bHLH transcription factor regulates early xylem Hamann T, Benkova E, Baurle I, Kientz M, Jurgens G development downstream of auxin. Plant Cell Physiol (2002) The Arabidopsis BODENLOS gene encodes an 54: 398–405 auxin response protein inhibiting Ohashi-Ito K, Oguchi M, Kojima M, Sakakibara H, Fukuda MONOPTEROS-mediated embryo patterning. Genes H (2013b) Auxin-associated initiation of vascular cell Dev 16: 1610–1615 differentiation by LONESOME HIGHWAY. Hardtke CS, Berleth T (1998) The Arabidopsis gene Development 140: 765–769 MONOPTEROS encodes a transcription factor Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, mediating embryo axis formation and vascular Clark SE (2005) Class III homeodomain-leucine zipper development. EMBO J 17: 1405–1411 gene family members have overlapping, antagonistic, Mah¨ onen¨ AP, Bonke M, Kauppinen L, Riikonen M, Benfey and distinct roles in Arabidopsis development. Plant PN, Helariutta Y (2000) A novel two-component hybrid Cell 17: 61–76 molecule regulates vascular morphogenesis of the Raven PH, Evert RF, Eichhorn SE (1999) Biology of Plants, Arabidopsis root. Genes Dev 14: 2938–2943 6th Edn. W.H. Freeman and Company, New York

132 Physiol. Plant. 151, 2014 Scacchi E, Osmont KS, Beuchat J, Salinas P, Smith ZR, Long JA (2010) Control of Arabidopsis Navarrete-Gomez M, Trigueros M, Ferrandiz C, Hardtke apical-basal embryo polarity by antagonistic CS (2009) Dynamic, auxin-responsive plasma transcription factors. Nature 464: 423–426 membrane-to-nucleus movement of Arabidopsis BRX. Song SK, Hofhuis H, Lee MM, Clark SE (2008) Key Development 136: 2059–2067 divisions in the early Arabidopsis embryo require POL Scacchi E, Salinas P, Gujas B, Santuari L, Krogan N, Ragni and PLL1 phosphatases to establish the root stem cell L, Berleth T, Hardtke CS (2010) Spatio-temporal organizer and vascular axis. Dev Cell 15: 98–109 sequence of cross-regulatory events in root meristem Steinmann T, Geldner N, Grebe M, Mangold S, Jackson growth. Proc Natl Acad Sci USA 107: 22734–22739 CL, Paris S, Galweiler L, Palme K, Jurgens¨ G (1999) Scarpella E, Helariutta Y (2010) Vascular pattern formation Coordinated polar localization of auxin efflux carrier in plants. Curr Top Dev Biol 91: 221–265 PIN1 by GNOM ARF GEF. Science 286: 316–318 Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of Talbert PB, Adler HT, Parks DW, Comai L (1995) The leaf vascular patterning by polar auxin transport. Genes REVOLUTA gene is necessary for apical meristem Dev 20: 1015–1027 development and for limiting cell divisions in the leaves Scheres B, Wolkenfelt H, Willemsen V, Terlouw M, and stems of Arabidopsis thaliana. Development 121: Lawson E, Dean C, Weisbeek P (1994) Embryonic origin 2723–2735 of the Arabidopsis primary root and root meristem Truernit E, Bauby H, Belcram K, Barthelemy J, Palauqui JC initials. Development: 2475–2487 (2012) OCTOPUS, a polarly localised Scheres B, Laurenzio LD, Willemsen V, Hauser MT, membrane-associated protein, regulates phloem Janmaat K, Weisbeek P, Benfey PN (1995) Mutations differentiation entry in Arabidopsis thaliana. affecting the radial organisation of the Arabidopsis root Development 139: 1306–1315 display specific defects throughout the embryonic axis. Weijers D, Schlereth A, Ehrismann JS, Schwank G, Kientz Development 121: 53–62 M, Jurgens G (2006) Auxin triggers transient local Schlereth A, Moller B, Liu W, Kientz M, Flipse J, signaling for cell specification in Arabidopsis Rademacher EH, Schmid M, Jurgens G, Weijers D embryogenesis. Dev Cell 10: 265–270 (2010) MONOPTEROS controls embryonic root Williams L, Grigg SP, Xie M, Christensen S, Fletcher JC initiation by regulating a mobile transcription factor. (2005) Regulation of Arabidopsis shoot apical meristem Nature 464: 913–916 and lateral organ formation by microRNA miR166g and Schrick K, Mayer U, Horrichs A, Kuhnt C, Bellini C, Dangl its AtHD-ZIP target genes. Development 132: J, Schmidt J, Jurgens G (2000) FACKEL is a sterol C-14 3657–3668 reductase required for organized cell division and expansion in Arabidopsis embryogenesis. Genes Dev 14: 1471–1484

Edited by Y. Helariutta

Physiol. Plant. 151, 2014 133