Stem cell function during plant vascular development
2012; Springer Nature; Volume: 32; Issue: 2 Linguagem: Inglês
10.1038/emboj.2012.301
ISSN1460-2075
AutoresShunsuke Miyashima, José Sebastián, Ji‐Young Lee, Ykä Helariutta,
Tópico(s)Plant Reproductive Biology
ResumoReview20 November 2012free access Stem cell function during plant vascular development Shunsuke Miyashima Shunsuke Miyashima Department of Bio and Environmental Sciences, Institute of Biotechnology, University of Helsinki, Helsinki, Finland Search for more papers by this author Jose Sebastian Jose Sebastian Boyce Thompson Institute for Plant Research, Ithaca, NY, USA Search for more papers by this author Ji-Young Lee Ji-Young Lee Boyce Thompson Institute for Plant Research, Ithaca, NY, USA Department of Biological Sciences, Seoul National University, Seoul, Korea Search for more papers by this author Yka Helariutta Corresponding Author Yka Helariutta Department of Bio and Environmental Sciences, Institute of Biotechnology, University of Helsinki, Helsinki, Finland Search for more papers by this author Shunsuke Miyashima Shunsuke Miyashima Department of Bio and Environmental Sciences, Institute of Biotechnology, University of Helsinki, Helsinki, Finland Search for more papers by this author Jose Sebastian Jose Sebastian Boyce Thompson Institute for Plant Research, Ithaca, NY, USA Search for more papers by this author Ji-Young Lee Ji-Young Lee Boyce Thompson Institute for Plant Research, Ithaca, NY, USA Department of Biological Sciences, Seoul National University, Seoul, Korea Search for more papers by this author Yka Helariutta Corresponding Author Yka Helariutta Department of Bio and Environmental Sciences, Institute of Biotechnology, University of Helsinki, Helsinki, Finland Search for more papers by this author Author Information Shunsuke Miyashima1,‡, Jose Sebastian2,‡, Ji-Young Lee2,3 and Yka Helariutta 1 1Department of Bio and Environmental Sciences, Institute of Biotechnology, University of Helsinki, Helsinki, Finland 2Boyce Thompson Institute for Plant Research, Ithaca, NY, USA 3Department of Biological Sciences, Seoul National University, Seoul, Korea ‡These authors contributed equally to this work. *Corresponding author. Department of Bio and Environmental Sciences, Institute of Biotechnology, University of Helsinki, Helsinki 00014, Finland. Tel.: +358 9 191 59432; Fax: +358 9 191 597788; E-mail: [email protected] The EMBO Journal (2013)32:178-193https://doi.org/10.1038/emboj.2012.301 PDFDownload PDF of article text and main figures. ToolsAdd to favoritesDownload CitationsTrack CitationsPermissions ShareFacebookTwitterLinked InMendeleyWechatReddit Figures & Info The plant vascular system, composed of xylem and phloem, evolved to connect plant organs and transport various molecules between them. During the post-embryonic growth, these conductive tissues constitutively form from cells that are derived from a lateral meristem, commonly called procambium and cambium. Procambium/cambium contains pluripotent stem cells and provides a microenvironment that maintains the stem cell population. Because vascular plants continue to form new tissues and organs throughout their life cycle, the formation and maintenance of stem cells are crucial for plant growth and development. In this decade, there has been considerable progress in understanding the molecular control of the organization and maintenance of stem cells in vascular plants. Noticeable advance has been made in elucidating the role of transcription factors and major plant hormones in stem cell maintenance and vascular tissue differentiation. These studies suggest the shared regulatory mechanisms among various types of plant stem cell pools. In this review, we focus on two aspects of stem cell function in the vascular cambium, cell proliferation and cell differentiation. Introduction A stem cell is a self-renewing cell whose progeny has a competence to differentiate into diverse ranges of specialized cell types. By classical definition, a stem cell is characterized by asymmetric cell division in which one daughter cell retains the characteristics of an undifferentiated mother cell and the other acquires a specific cell fate, which is triggered by intrinsic and extrinsic signals. Stem cells maintain their pluripotent status in special microenvironments, called ‘stem cell niche’, together with niche cells (Spradling et al, 2001). Niche cells send out short-range signals that are required for stem cell maintenance. The concept of stem cell niche was first proposed in mammalian haematopoietic tissue and has been extended to various types of stem cells (Fuchs et al, 2004; Li and Li, 2006). Plants continue to grow in apical and lateral directions, forming new cells and organs throughout their life cycle. Cell division that promotes these growth activities is concentrated in meristems, specialized domains that maintain actively dividing undifferentiated cells. Meristems provide a microenvironment that protects the stem cell niche, thereby acts as a central place for growth and development (reviewed by Scheres, 2007). The shoot apical meristem (SAM) and the root apical meristem (RAM), located at the apices of main and lateral shoots and roots, produce cells for lateral organ formation and tip growth (Figure 1A, B and D). The number of stem cells within SAM and RAM is tightly maintained by mechanisms that balance between cell division and cell differentiation. The SAM is divided into three different zones: the peripheral zone (PZ), the central zone (CZ) and the rib zone (RZ) (Figure 1A). In the CZ, pluripotent stem cells and the organizing centre (OC) together form a stem cell niche (Figure 1A). These stem cells continuously produce daughter cells by asymmetric cell division, and their daughter cells, subsequently displaced to the PZ, are recruited into lateral organ primordia (Tucker and Laux, 2007). In the RAM, the stem cells are present as a single cell layer that surrounds the quiescent centre (QC), and their daughter cells are committed into specific cell fates depending on their position (Figure 1B; Van den berg et al, 1995). In apical meristems, the OC and QC act as niche cells that maintain adjacent stem cells (Laux et al, 1996; Mayer et al, 1998; Fletcher et al, 1999; Schoof et al, 2000; Sarkar et al, 2007; Stahl et al, 2009). Figure 1.Regulation of stem cells and their niches in Arabidopsis. (A–C) The organization of stem cell niche in shoot apical meristem (SAM) (A), root apical meristem (RAM) (B) and vascular cambium (C), and their WUS-CLV regulatory mechanism in each meristem. In SAM and RAM, the stem cells are adjacent to the niche cells, which maintain their pluripotency (A, B). In RAM, daughter cells of stem cells are committed into specific cell fates depending on their position (B). (D) The location of SAM and RAM is indicated in 5-day-old Arabidopsis seedling. Download figure Download PowerPoint In addition to stem cells in the SAM and RAM, vascular stem cells, or more commonly called procambium and cambium are formed in vascular plants (Figures 1C and 2A). This pool of stem cells continuously produces xylem and phloem, major plant vascular tissues. Plant vascular tissues provide physical strength to plant bodies and transport water, nutrients and other substances required for growth and defense. They interconnect all the plant body parts by their conductive function, from the root tip to the various organs in the shoot. Xylem is the main tissue for transporting water and solute minerals, whereas phloem is the route for distributing photosynthetic products and various signalling molecules. Vascular stem cells generate these two conductive tissues via asymmetric periclinal cell division (Eames and MacDaniels, 1947; Esau, 1965). Figure 2.Organization of vascular tissues in Arabidopsis root and Populus stem. (A) A schematic cross-section of Arabidopsis root showing the vascular organization during the primary development. (B, C) Cross-sections of Arabidopsis root (B) and Populus stem (C) during the secondary development. Download figure Download PowerPoint Gymnosperms and many dicotyledons undergo two distinct phases of growth and development (Eames and MacDaniels, 1947; Esau, 1965). The primary growth increases plant biomass mainly in the apical direction while the secondary growth does in the lateral direction. During primary growth, xylem and phloem differentiate from cells that are derived from intervening procambium. Once the primary vascular tissues are established, cambium is generated from procambium and its neighbouring cells in stems and roots where it promotes the secondary growth. Cell proliferation in the cambium is usually more active than the one in the procambium (Eames and MacDaniels, 1947; Esau, 1965). An increase in the amount of vascular tissues mediated by cambium is one of the characteristics that distinguish dicotyledons and gymnosperms from monocots. In most monocots, all the procambial cells appear to differentiate into vascular tissues during primary growth. As a result, the cambium does not form and the secondary growth does not occur in these plants (Esau, 1965). The procambium and the cambium may be considered as the same set of vascular stem cells at two developmental stages, because their basic characteristics are very similar. For instance, both procambium and cambium are the source of xylem and phloem. Furthermore, the morphology of procambial cells gradually becomes similar to cambial cells’ as both become vacuolated (Esau, 1965). Currently, however, we lack an understanding of the precise developmental transition from procambium to cambium. Cell division and differentiation in the cambium lead to the thickening of stems and roots and thereby increase the biomass. Since the secondary growth massively occurs especially in woody plants, its research has been traditionally focusing on tree species. However, the secondary growth is also observed in many herbaceous plants, and it results in the tissue organization very similar to that in tree species (Figure 2B and C). With several advantages such as genomic resources, Arabidopsis has emerged as a useful model for investigating the secondary growth. In particular, Arabidopsis root is an excellent model system for studying vascular development in the primary and the secondary growth because it is simpler and more predictable than the vascular development in other organs (Mahonen et al, 2000, 2006a; Matsumoto-Kitano et al, 2008; Carlsbecker et al, 2010). With the advancement in genomics and other molecular tools, our knowledge regarding the vascular development, such as the formation of vascular stem cells and subsequent differentiation into xylem and phloem, has rapidly expanded in recent years. Among them, significant progress has been made in studies on the role of phytohormones during the vascular development. Several phytohormones, such as auxin, cytokinin, gibberellins (GAs), ethylene and brassinosteroids, have been shown to regulate various aspects of vascular morphogenesis (Tuominen et al, 1997; Scarpella et al, 2006; Nilsson et al, 2008; Matsumoto-Kitano et al, 2008; Ibañes et al, 2009; Mauriat and Moritz, 2009). Recent molecular genetic studies in Arabidopsis and Populus and cellular studies with Zinnia xylogenic cell culture have started to reveal the molecular mechanisms underlying phytohormone action in vascular development (Ohashi-Ito et al, 2002; Schrader et al, 2004b; Mahonen et al, 2006a; Scarpella et al, 2006). In addition, several transcription factors involved in the vascular stem cell maintenance have been identified. These findings suggest the existence of conserved regulatory programs among different plant stem cell pools (reviewed by Sablowski, 2011). Vascular stem cells: initiation and primary development The initiation of vascular stem cells during embryogenesis is well characterized in Arabidopsis. At the early globular stage of Arabidopsis embryos, cells inside the protoderm divide into distinct layers, the ground tissue precursors and vascular stem cell initials (procambium) (Figure 3A; Mansfield and Briarty, 1991; Lau et al, 2010). At the late globular stage, four procambial cells divide periclinally, giving rise to the pericycle and vascular stem cells. During the late globular, heart and torpedo stages, the number of cell files in the procambium continues to increase by further periclinal cell divisions resulting in the radial vascular pattern identical to that of a post-embryonic primary root (Scheres et al, 1994; Mahonen et al, 2000). Figure 3.The initiation and formation of procambium cells is regulated by the auxin-mediated positive feedback loop. (A) Schemes of longitudinal median sections during early embryogenesis in Arabidopsis. (B) The polar localization of PIN1 and the expression pattern of MP during early Arabidopsis embryogenesis. (C) The auxin-mediated regulatory loop controlling the vascular initiation during leaf vein growth. Download figure Download PowerPoint Simultaneously, a network of vascular stem cells arises in cotyledons as well. Although a continuous procambial tissue extends in an apical-basal axis without exhibiting any feature of differentiated vascular elements in a mature embryo, several vascular tissue-specific markers are reported to be expressed at this developmental stage, indicating that vascular cell fate decisions are already made during embryogenesis (Bonke et al, 2003; Mahonen et al, 2006a). Over the years numerous genetic studies have revealed several genes involved in the radial patterning during Arabidopsis embryogenesis (reviewed by Jenik et al, 2007 and Lau et al, 2012). Among them, a pair of LRR receptor-like kinases, RECEPTOR-LIKE PROTEIN KINASE1 (RPK1) and TOADSTOOL2 (TOAD2), seems to be involved in the determination of the procambium position during early embryogenesis (Table I; Nodine et al, 2007). Both of these genes start to be expressed in the early globular stage. Embryo development in the rpk1 toad2 double mutant is arrested at the late globular stage. Interestingly, in the rpk1 toad2 embryo, the expression of procambial marker genes expands beyond procambium cells into ground tissue initials and protoderm, while the expression of markers for protoderm and ground tissue is severely attenuated. This indicates that these two LRR receptor-like kinases regulate positioning and patterning of the early procambium in the embryo (Nodine et al, 2007). Table 1. List of genes that regulate vascular stem cells Gene name Description Function References RECEPTOR-LIKE PROTEIN KINASE1 (RPK1) LRR-receptor kinase Determination of procambium position in Arabidopsis embryo Nodine et al (2007) TOADSTOOL2 (TOAD2) LRR-receptor kinase Determination of procambium position in Arabidopsis embryo Nodine et al (2007) MONOPTEROS (MP) Auxin responsive transcription factor Auxin response, vascular stem cell initiation Hardtke and Berleth (1998); Scarpella et al (2006); Donner et al (2009) PIN-FORMED1 (PIN1) Auxin efflux carrier Polar auxin transport, vascular stem cell initiation Hardtke and Berleth (1998); Scarpella et al (2006); Donner et al (2009) ARABIDOPSIS THALIANA HOMEOBOX 8 (ATHB8) Class III homeodomain-leucine zipper Xylem formation, targeted by microRNA165/166 Baima et al (2001); Carlsbecker et al (2010); Donner et al (2009); Hardtke and Berleth (1998); Scarpella et al (2006) SCARFACE (SFC) ARF-GAP protein PIN protein recycling; affects vein growth Deyholos et al (2000); Koizumi et al (2005); Sieburth et al (2006) Xylogen (XYP1/2) Proteoglycan-like protein Affects the continuity of xylem networks Motose et al (2004) OCTOPUS (OPS) Membrane localized protein Affects the continuity of phloem networks Truernit et al (2012) PHABULOSA (PHB) Class III homeodomain-leucine zipper Xylem formation, targeted by microRNA165/166 Carlsbecker et al (2010) PHAVOLUTA (PHV) Class III homeodomain-leucine zipper Xylem formation, targeted by microRNA165/166 Carlsbecker et al (2010) REVOLUTA (REV) Class III homeodomain-leucine zipper Formation of interfascicular fibres, xylem formation, targeted by microRNA165/166 Carlsbecker et al (2010) CORONA (CNA) Class III homeodomain-leucine zipper Xylem formation, targeted by microRNA165/166 Carlsbecker et al (2010) KANADI (KAN) GARP family protein, putative transcription factor Antagonistic role to class III homeodomain-leucine zipper Emery et al (2003); Ilegems et al (2010) SHORT ROOT (SHR) GRAS type transcription factor Endodermis formation, regulatin microRNA165/166 in root Carlsbecker et al (2010) SCARECROW (SCR) GRAS type transcription factor Endodermis formation, regulatin microRNA165/166 in root Carlsbecker et al (2010) VASCULAR-RELATED NAC-DOMAIN 6/7 NAC transcription factor Vessel formation Kubo et al (2005) ALTERD PHLOEM DEVELOPMENT (APL) MYB coiled-coil-type transcription factor Phloem differentiation Bonke et al (2003) HIGH CAMBIAL ACTIVITY 2 (HCA2) Dof type transcription factor Cell proliferation and phloem formation in cambium Guo et al (2009) Pta LBD1 LBD/ASL family protein Cell proliferation in cambium Yordanov et al (2010) ARK1/2 Class I KNOTTED1-like homeobox (KNOX) transcription factor Cell proliferation in cambium Du et al (2009); Groover et al (2006) WUSCHEL-like HOMEOBOX 4 (WOX4) Homeobox transcription factor Stem cell maintenance in cambium Hirakawa et al (2010b); Suer et al (2011) CLAVATA3/ESR-related 41/44 (CLE41/44) Peptide ligand Stem cell maintenance in cambium Hirakawa et al (2008); Whitford et al (2008) PHLOEM INTERCALATED WITH XYLEM (PXY)/TDIF RECEPTOR (TDR) LRR-receptor kinase Stem cell maintenance in cambium Fisher and Turner (2007); Hirakawa et al (2008) MORE LATERAL GROWTH 1 (MOL1) LRR-receptor kinase Regulating cell proliferation in interfascicular cambium Agusti et al (2011b) REDUCED IN LATERAL GROWTH 1 (RUL1) LRR-receptor kinase Regulating cell proliferation in interfascicular cambium Agusti et al (2011b) CYTOKININ RESPONSE 1 (CRE1)/WOODEN LEG (WOL)/ARABIDOPSIS HISTIDINE KINASE (AHK) Histidine kinase, cytokinin receptor Cytokinin receptor, stem cell maintenance in procambium/cambium by inhibiting xylem differentiation Mahonen et al (2000) AHP6 A pseudo-phosphotransfer protein Cytokinin signalling, protoxylem specification Mahonen et al (2006a) ARR1, 10 and 12 Type B ARRs Cytokinin signalling, inhibit the differentiation of procambium into xylem Argyros et al (2008); Hutchison et al (2006); Ishida et al (2008); Yokoyama et al (2007) ISOPENTENYLTRANSFERASE (IPT) ISOPENTENYLTRANSFERASE Cytokinin biosynthesis, promote cambium activity Matsumoto-Kitano et al (2008) BRI1, BRL1-3 LRR-receptor kinase Brassinosteroid receptor, promote xylem development Cano-Delgado et al (2004); Nakamura et al (2006); Yamamoto et al (2001, 2007) GA 20-oxidase GIBBERELLIN 3-OXIDASE Gibberellin biosynthesis, promote a cambium activity and the formation of xylem fibres Israelsson et al (2005) GA 3-oxidase GIBBERELLIN 20-OXIDASE Gibberellin biosynthesis, promote a cambium activity and the formation of xylem fibres Israelsson et al (2005) JASMONATE ZIM-DOMAIN (JAZ) 7 and 10 Jasmonate ZIM-domain protein Jasmonates signalling, jasmonates receptor, repress cambial activities by inhibiting MYC2 Chini et al (2007); Sehr et al (2010); Thines et al (2007) CORONATINE INSENSITIVE1 (COI1) F-box protein Jasmonates signalling, jasmonates receptor Chini et al (2007); Sehr et al (2010); Thines et al (2007) MYC2 MYC related transcription factor Induced by jasmonates, promotes cambial activities Chini et al (2007); Sehr et al (2010); Thines et al (2007) ERF104 ETHYLENE RESPONSE FACTOR Promote interfascicular cambium initiation Bethke et al (2009) The importance of auxin in vascular stem cell initiation has been demonstrated in several studies using Arabidopsis as a model system (Table I; reviewed by Reinhardt, 2003). An auxin responsive transcription factor, MONOPTEROS (MP)/AUXIN RESPONSE FACTOR5 (ARF5), plays a critical role in the specification of vascular stem cells (Hardtke and Berleth, 1998). During early embryogenesis, MP is expressed in the procambial cells and its expression is rapidly upregulated by auxin (Figure 3B). In mp knockout mutant embryos, procambium completely fails to form and weak alleles display irregular vascular development (Berleth and Jurgens, 1993; Hardtke and Berleth, 1998). Such a defect seems to be related to the lack of polar auxin transport during embryogenesis. During early embryogenesis, PIN-FORMED1 (PIN1) proteins, major auxin efflux carriers, are polarly localized in the inner cells of pro-embryo before they turn into procambial cells (Figure 3B; Friml, 2003). PIN1 expression is dramatically reduced in a loss-of-function mp mutant, suggesting that MP might regulate its transcription (Wenzel et al, 2007). In early stages of leaf development, preprocambial cells, from a sub-epidermal layer of leaf primordia, are organized into continuous strands to form veins, networks of vascular tissues (Eames and MacDaniels, 1947). Unlike stem cells in the SAM or RAM, vascular stem cells in developing leaves are constantly formed to produce vein networks. Therefore, the proper vein growth requires the same molecular processes involved in the vascular stem cell formation in an iterative manner. One key question in the vein growth is how procambial cells signal from one to the other to form continuous vascular strands. The auxin-canalization hypothesis has been proposed to explain this (Sachs, 1981; Rolland-Lagan and Prusinkiewicz, 2005). According to this hypothesis, the vein growth is promoted via a positive feedback regulation of auxin transport. More specifically, the auxin maxima established in procambial cells enhance the machinery that transports auxin to adjacent cells in a polar manner. The adjacent cells that subsequently perceive a high level of auxin turn into procambium and repeat the same process to the next neighbours. The auxin canalization theory was supported by the findings of the auxin efflux carrier protein, PIN1. In pin1 mutant stems, the arrangement of vascular bundles is abnormal, similar to when the auxin transport inhibitor is applied (Gälweiler et al, 1998). PIN1 expression was further characterized in developing leaves (Scarpella et al, 2006). This study showed that PIN1 starts to be expressed in the vascular stem cells before they become morphologically discernible. Then, expression domains of PIN1 expanded to the future veins as leaf primordia emerged and grew. When the veins were about to bifurcate, PIN1 localization became bipolar in the bifurcating cell. These suggest that polar auxin transport is vital for the proper organization of vascular stem cells. The auxin canalization theory proposes that the positive feedback regulation of auxin transport is required for the auxin maxima to be established in the preprocambial cells of growing veins. Recent genetic studies revealed the molecular basis of such regulation (reviewed by Scarpella et al, 2010). One of the earliest expressing transcriptional regulators in the preprocambial cells is the ARABIDOPSIS THALIANA HOMEOBOX8 (ATHB8), a class III homeo-domain leucine zipper (HD-ZIP III) transcription factor family gene (Table I; Donner et al, 2009). It turned out that the transcription of ATHB8 is activated directly by MP. ATHB8 subsequently directs the formation of preprocambial cells and induces the expression of PIN1 (Figure 3C; Scarpella et al, 2006). These processes establish a positive feedback loop of auxin-MP-ATHB8-PIN1 in the initiation and specification of vascular stem cells. When this positive feedback regulation was disrupted in the athb8 mutant, the expression domain of a preprocambium marker (J1721) expanded. This supports the importance of positive feedback regulation for spatially restricting preprocambial cell specification (Donner et al, 2009). PIN proteins cycle between plasma membranes and endosomes via the activity of ARF–GEF protein, GNOM (Geldner et al, 2003). The importance of polar auxin transport in vein growth and patterning was further evident from mutations in components of PIN localization machinery. For example, scarface (sfc)/van3 generates dense but fragmented vein islands on leaves and cotyledons. SFC encodes an ADP ribosylation factor GTPase activating protein (ARF–GAP), a modulator of ARF–GEF, involved in the vesicle trafficking (Deyholos et al, 2000; Koizumi et al, 2005; Sieburth et al, 2006). In the sfc, intracellular trafficking of PIN1 was abnormal, suggesting that SFC might affect the endosomal cycling of PIN1 (Sieburth et al, 2006). Other factors involved in vascular continuity have also been reported (Table I). Among them, Xylogen, a large proteoglycan-like protein (Motose et al, 2004), is polarly localized in the cell walls of differentiating tracheary elements to function as an intercellular signal molecule. The Arabidopsis genome contains two genes encoding Xylogen, AtXYP1 and AtXYP2. When these two are knocked out xylem strands develop in a discontinuous manner (Motose et al, 2004). OCTOPUS, a polarly localized membrane-associated protein in the phloem, has been reported to regulate phloem continuity in Arabidopsis (Truernit et al, 2012). Besides ATHB8, the Arabidopsis genome contains four other HD-ZIP III genes PHABULOSA (PHB), PHAVOLUTA (PHV), REVOLUTA/INTERFASCICULAR FIBERLESS1 (REV/IFL1), CORONA (CNA)/ATHB15 (Table I) (Talbert et al, 1995; Baima et al, 2001; McConnell et al, 2001; Green et al, 2005; Prigge et al, 2005). All of them are expressed in vascular tissues in somewhat overlapping fashion, suggesting a likely redundancy in their function (Prigge et al, 2005; Carlsbecker et al, 2010). A quadruple knockout mutant for ATHB8, CNA, PHB and PHV was reported to exhibit enhanced cell proliferation in procambium (Carlsbecker et al, 2010). Furthermore, a quintuple mutant, athb8-11 cna-2 phb-13 phv-11 rev-6, completely lacked xylem, highlighting their involvement in the vascular cell type specification (Carlsbecker et al, 2010). The KANADI (KAN) genes, a subclass of GARP family transcription factors, have been shown to play an antagonistic role to HD-ZIP III genes in dorsoventral patterning of lateral organs (Emery et al, 2003). In the vascular tissue of a quadruple loss-of-function KANADI mutant (kan1 kan2 kan3 kan4), the cell proliferation in procambium was strikingly enhanced (Ilegems et al, 2010). On the contrary, ectopic expression of KAN1 under the CNA/ATHB15 promoter suppressed PIN1 expression in procambium during embryogenesis and thereby repressed the vascular stem cell initiation (Ilegems et al, 2010). This finding indicates that KAN genes might antagonize HD-ZIP III genes through the modulation of PIN1 expression. Interestingly, KAN genes are expressed in the phloem, thus they might control vascular stem cell development in a non-cell autonomous manner (Emery et al, 2003). In summary, a positive feedback loop of auxin-MP-PIN1 mediated by HD-ZIP III and KAN genes primarily controls the initiation and specification of vascular stem cells. Establishment of vascular cambium during the secondary development The cambium or vascular cambium represents a pool of stem cells arranged in radial series and gives rise to xylem and phloem cells during the secondary phase of plant development (Figures 2 and 4; Eames and MacDaniels, 1947; Esau, 1965). In stems, the procambium derived from apical meristem usually resides within the bundles (Eames and MacDaniels, 1947). During the secondary growth phase, the procambial cells become the ‘fascicular cambium’, the cambium derived from a vascular bundle of primary development (Figure 4). The clusters of fascicular cambium become interconnected by the ‘interfascicular cambium’, which is formed from parenchyma cells between the vascular bundles (Eames and MacDaniels, 1947), thereby completing the radial arrangement of cambium (Figure 4). The development of xylem in Arabidopsis can be divided into two distinct phases, based on which cell types differentiate from cambial cells. In an early phase, only vessel elements differentiate, and the rest of the xylem cells remain as parenchyma. At a later phase, both vessel elements and lignified fibre cells are produced from cambial cells, resulting in a stem anatomy comparable to wood of an angiosperm tree (Chaffey et al, 2002). Although numerous histological analyses in several plant species have revealed the dynamic morphological changes during the secondary development (Esau, 1965; Eames and MacDaniels, 1947), little is known about the molecular mechanisms underlying these processes. A loss-of-function mutation in REV leads to the disrupted development of xylem fibres and vessel elements in Arabidopsis, indicating a role for REV during the secondary phase of vascular development (Zhong and Ye, 1999). Figure 4.Schematic illustration of the primary and secondary stem anatomy in Arabidopsis. The primary stem exhibits disconnected vascular bundles with procambium. In the secondary developmental phase, this procambium turns into a fascicular cambium and the cells between bundles become an interfascicular cambium. Fascicular and interfascicular cambia interconnect to each other and establish a cambium in a circular form. Download figure Download PowerPoint The vascular cambium enlarges its circumference through anticlinal cell divisions (occur perpendicular to an adjacent cell layer), while it continues to undergo periclinal cell divisions (occur parallel to an adjacent cell layer) to produce mother cells for xylem and phloem (Figure 4). The vascular cambium contains two types of cells: elongated cells with tapering ends, the fusiform initials (spindle-shaped initials), and the ray initials, which are nearly isodiametric and relatively small in size. The fusiform initials upon differentiation give rise to xylem and phloem, while the ray initials give origin to the radial strands of cubical cells that play a rol
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