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CB26CH24-Cano-Delgado ANNUAL REVIEWS ARI 3 September 2010 Further Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. Click here for quick links to Annual Reviews content online, including: • Other articles in this volume • Top cited articles • Top downloaded articles • Our comprehensive search 20:17 Regulatory Mechanisms for Specification and Patterning of Plant Vascular Tissues Ana Caño-Delgado,1,∗ Ji-Young Lee,2,3,∗ and Taku Demura4,5,∗ 1 Molecular Genetics Department, Center for Research in Agricultural Genomics, Barcelona 08034, Spain; email: [email protected] 2 Boyce Thompson Institute for Plant Research, Ithaca, NY 14853; email: [email protected] 3 Department of Plant Biology, Cornell University, Ithaca, NY 14853 4 RIKEN Plant Science Center, Yokohama, Kanagawa 230-0045, Japan 5 Graduate School of Biological Sciences, Nara Institute of Science and Technology, Ikoma, Nara 630-0136, Japan; email: [email protected] Annu. Rev. Cell Dev. Biol. 2010. 26:605–37 Key Words First published online as a Review in Advance on June 29, 2010 vascular, procambium, xylem, phloem, auxin, brassinosteroids, regulatory networks The Annual Review of Cell and Developmental Biology is online at cellbio.annualreviews.org This article’s doi: 10.1146/annurev-cellbio-100109-104107 c 2010 by Annual Reviews. Copyright All rights reserved 1081-0706/10/1110-0605$20.00 ∗ These authors contributed equally to this work. Abstract Plant vascular tissues, the conduits of water, nutrients, and small molecules, play important roles in plant growth and development. Vascular tissues have allowed plants to successfully adapt to various environmental conditions since they evolved 450 Mya. The majority of plant biomass, an important source of renewable energy, comes from the xylem of the vascular tissues. Efforts have been made to identify the underlying mechanisms of cell specification and patterning of plant vascular tissues and their proliferation. The formation of the plant vascular system is a complex process that integrates signaling and gene regulation at transcriptional and posttranscriptional levels. Recently, a wealth of molecular genetic studies and the advent of cell biology and genomic tools have enabled important progress toward understanding its underlying mechanisms. Here, we provide a comprehensive review of the cell and developmental processes of plant vascular tissue and resources recently available for studying them that will enable the discovery of new ways to develop sustainable energy using plant biomass. 605 CB26CH24-Cano-Delgado ARI 3 September 2010 20:17 Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. Contents VASCULAR TISSUE SPECIFICATION AND PATTERNING . . . . . . . . . . . . . . . . . Initiation of Vascular Tissues in Developing Embryos . . . . . . . . . . Postembryonic Development of Vascular Tissues . . . . . . . . . . . . . . Vascular Tissue Formation During Plant Growth: Venation . . . . . . . Vascular Tissue Formation During Plant Growth: Secondary Growth . . . . . . . . . . . . . . . . . . . . . . . Vascular Cell Type Specification and Gene Expression . . . . . . . . . . HORMONAL REGULATION OF VASCULAR TISSUE/CELL SPECIFICATION . . . . . . . . . . . . . . . The Roles of Auxin in Vascular Cell Differentiation . . . . . . . . . . . . Auxin Transport in Vascular Patterning . . . . . . . . . . . . . . . . . . . . Brassinosteroid Signaling During Vascular Development . . . . . . . . . Cytokinins During Vascular Cell Differentiation . . . . . . . . . . . . . . . . 606 606 607 612 612 613 616 616 617 618 621 VASCULAR TISSUE SPECIFICATION AND PATTERNING Plant vascular system: a complex of conducting tissues composed of xylem, phloem, and procambium/cambium Xylem: waterconducting tissue composed of xylem vessel elements (more generally tracheary elements), fibers, and other metabolic cells (called parenchymas) 606 Initiation of Vascular Tissues in Developing Embryos The prepatterning of the plant vascular system in developing embryos provides an important stepping stone toward postembryonic patterning and growth of vascular tissues and their associated organs. Immediately after fertilization, zygotes divide three times in an isodiametric manner. After reaching the octant stage, the cells in the lower tier proliferate differentially from those in the upper tier, generating elongated cells in the lower middle part of the embryo (Berleth & Caño-Delgado · · Lee Demura TRANSCRIPTIONAL REGULATION OF VASCULAR CELL SPECIFICATION . . . . . . . . HD-ZIP III/KAN/microRNA System Responsible for Early Vascular Development . . . . . . . . . Positive Regulators of Xylem Cell Specification . . . . . . . . . . . . . . . . . . Fine-Tuning of Gene Expression During Xylem Cell Specification . . . . . . . . . . . . . . . . . . Regulators of Phloem Cell Specification . . . . . . . . . . . . . . . . . . TOWARD COMPREHENSIVE REGULATORY NETWORKS AND SIGNALING IN VASCULAR TISSUE SPECIFICATION AND PATTERNING . . . . . . . . . . . . . . . . . Cell Biology Resources: Vascular Cell Type–Specific Markers . . . . Theoretical Modeling for the Study of Vascular Patterning . . . Toolkits for the Understanding of Vascular Cell Specification and Differentiation . . . . . . . . . . . . 622 623 623 624 625 625 625 628 628 Jurgens 1993, Busse & Evert 1999a, Hardtke & Berleth 1998). These elongated cells that will become procambium cells further extend in the apical direction toward the future cotyledons of early heart-stage embryos and create a single network of vascular precursors (Figure 1). In some species, xylem and phloem begin to differentiate from procambium in mature embryos, but in many others vascular tissue differentiation only starts after the seed germinates (Esau 1965, Sundberg 1983). Auxin regulates the initiation of procambial cells in the lower tier of the octant stage of embryos. In the absence of auxin signaling mediated by MONOPTEROS (MP), an auxinresponsive factor, procambial cells in embryos do not form properly (Berleth & Jurgens 1993, Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. CB26CH24-Cano-Delgado Zygote ARI 2-cell 3 September 2010 16-cell 20:17 Early globular Globular Early heart Figure 1 Establishment of the procambium during embryogenesis. At the globular stage, cells in the lower tier start elongation, whereas those in the upper tier ( yellow) stay isodiametric. These elongated cells ( purple) become procambium. Hardtke & Berleth 1998), which subsequently results in the failure of postembryonic growth of vascular tissues. Postembryonic Development of Vascular Tissues Although the vascular tissues are connected throughout the postembryonic plant body, their organization is distinctive in each organ. In the root, vascular tissues form a cylindrical structure that is consecutively surrounded by the radial tissues, pericycle, endodermis, cortex, and epidermis. Xylem develops in the center of the vascular cylinder and branches toward the pericycle. These xylem branches alternate with phloem (Figure 2). The organization of xylem branches and phloem tends to be unique to each species, suggesting that these characteristics are genetically controlled. A basic helix-loop-helix transcription factor (TF), LONESOME HIGHWAY, is a potential regulator of this vascular patterning (Ohashi-Ito & Bergmann 2007). Its knockout mutant generates only one pole of xylem and phloem (monoarch) instead of two poles (diarch) in Arabidopsis thaliana roots. Specification and differentiation of xylem vessel types in the root are temporally and spatially regulated (Table 1). Although the precursors of xylem are established in the root meristem, their differentiation does not start until the stage when roots actively elongate and develop hairs in the epidermis. Xylem vessel precursors on the periphery of the xylem axis differentiate earlier than those in the inner layers and differentiate into protoxylem, xylem vessels with spirally patterned secondary cell www.annualreviews.org • Plant Vascular Patterning Phloem: nutrientconducting tissue composed of phloem sieve cells and companion cells; protophloem and metaphloem constitute the primary phloem Procambium: the meristematic tissues from which xylem and phloem develop TF: transcription factor 607 CB26CH24-Cano-Delgado ARI 3 September 2010 Auxin 20:17 PIN1, SCF/VAN3, VAB MP ATHB-8 Adaxial Leaf Abaxial Stem Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. COV1, HCA, PXY, HD-ZIP III, ARBORKNOX1/2 Phloem mother cell Cambium Xylem mother cell Hypocotyl Cell growth Secondary cell wall formation Cell death CLE/PXY APL VND6 Root VND7 ? ? High HD-ZIP III miR165/166 Low HD-ZIP III SHR/SCR Pericycle Phloem sieve cells Phloem companion cells Epidermis Procambium/cambium Endodermis Quiescent center Endodermis/cortex initial Cortex Metaxylem vessel Protoxylem vessel Figure 2 Vascular tissue patterning during postembryonic growth and development, and representative regulators. Vascular tissues are connected as a single network in plants; however, their organization changes in different parts of a plant body. (left) How vascular tissues are connected in a plant body. (right) More detailed organizations of vascular tissues in leaf, stem, and root. Representative regulators or pathways in vascular patterning are listed in red boxes. APL, ALTERED PHLOEM DEVELOPMENT; ATHB-8, class III homeodomain transcription factor 8; CLE, CLAVATA3-like small protein ligands; COV1, CONTINUOUS VASCULAR RING 1; HD-ZIP III, class III homeodomain-leucine zipper; HCA, HIGH CAMBIAL ACTIVITY; miR, microRNA; MP, MONOPTEROS; PIN1, auxin efflux carrier; PXY, PHLOEM INTERCALATED WITH XYLEM; SCF/VAN3, SCARFACE; SCR, SCARECROW; SHR, SHORT ROOT; VAB, VAN3 binding protein; VND, VASCULAR-RELATED NAC-DOMAIN PROTEIN. 608 Caño-Delgado · · Lee Demura CB26CH24-Cano-Delgado Table 1 ARI 3 September 2010 Genes involved in vascular tissue development Gene name Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. 20:17 Gene family Function Reference PHABULOSA (PHB) HD-ZIP III TF Regulate xylem cell type patterning in the root; collateral vascular patterning in stems and leaves Emery et al. (2003), Itoh et al. (2008), Zhong & Ye (2004) PHAVOLUTA (PHV ) HD-ZIP III TF Regulate xylem cell type patterning in the root; collateral vascular patterning in stems and leaves Emery et al. (2003), Itoh et al. (2008), Zhong & Ye (2004) REVOLUTA (REV ) HD-ZIP III TF Regulate xylem cell type patterning in the root; collateral vascular patterning in stems and leaves Emery et al. (2003), Itoh et al. (2008), Zhong & Ye (2004) ATHB-8 HD-ZIP III TF Regulate xylem cell type patterning in the root; collateral vascular patterning in stems and leaves; leaf procambial cell growth in response to auxin Donner et al. (2009), Emery et al. (2003), Itoh et al. (2008), Zhong & Ye (2004) ATHB-15/CORONA (CNA) HD-ZIP III TF Regulate xylem cell type patterning in the root; collateral vascular patterning in stems and leaves Emery et al. (2003), Itoh et al. (2008), Zhong & Ye (2004) MONOPTEROS (MP) ARF Establishment of procambium during embryo- and postembryogenesis Berleth & Jurgens (1993), Hardtke & Berleth (1998) LONESOME HIGHWAY (LHW ) bHLH TF Vascular patterning in the root; mutant forms monoarch vasculature instead of diarch in the Arabidopsis root Ohashi-Ito & Bergmann (2007) SHORT ROOT (SHR) GRAS TF Regulate the xylem cell type patterning in the root by activating miR165/166 Carlsbecker et al. (2010) SCARECROW (SCR) GRAS TF Regulate the xylem cell type patterning in the root by activating miR165/166 Carlsbecker et al. (2010) ALTERED PHLOEM DEVELOPMENT (APL) Myb TF Phloem formation in the root; the mutant forms ectopic xylem in the phloem pole Bonke et al. (2003) CLE 41/44 CLAVATA3-like small protein ligands Inhibit vascular differentiation in the procambium Hirakawa et al. (2008), Whitford et al. (2008) PXY CLAVATA1-like LRR-receptor kinase Inhibit vascular differentiation in the procambium by binding to CLE 41/44; spatial patterning of vascular tissues in stems Fisher & Turner (2007), Hirakawa et al. (2008) CONTINUOUS VASCULAR RING 1 (COV1) a membrane-localized protein Regulate the density of vascular bundles in the stem Parker et al. (2003) SCARFACE (SFC) ARF-GAP Vein patterning by regulating the auxin transport pathway Deyholos et al. (2000), Koizumi et al. (2005), Sieburth et al. (2006) CVP2 inositol polyphosphate 5 -phosphatase Vein patterning by regulating the auxin transport pathway Carland & Nelson (2004), Carland et al. (2002) ARBORKNOX1 and 2 KNOX TF Repress the differentiation of vascular tissues Du et al. (2009) VND 6 NAC TF Promote metaxylem formation Kubo et al. (2005) VND 7 NAC TF Promote protoxylem formation Kubo et al. (2005) BRI1 LRR-receptor kinase Promote xylem differentiation and vascular bundle number Caño-Delgado et al. (2004) (Continued ) www.annualreviews.org • Plant Vascular Patterning 609 CB26CH24-Cano-Delgado Table 1 ARI 3 September 2010 (Continued ) Gene name Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. 20:17 Gene family Function Reference BRL1 LRR-receptor kinase Provascular-specific receptor that promotes xylem formation in the shoot inflorescence stem Caño-Delgado et al. (2004) BRL3 LRR-receptor kinase Phloem-specific receptor necessary to maintain collateral patterning of vascular bundles in the shoot inflorescence stem Caño-Delgado et al. (2004) VH1/BRL2 LRR-receptor kinase Provascular cell-specific receptor that affects leaf vasculature Clay & Nelson (2002) VIT VH1-interacting TPRcontaining protein Participates in initial stages of vascular strand formation Ceserani et al. (2009) VIK VH1-interacting kinase Participates in late stages of vascular strand formation Ceserani et al. (2009) WOODEN LEG (WOL)/ CRE1/AHK4 Histidine kinase (HK) receptor protein Cytokinin receptor necessary for early procambial cell divisions in embryogenesis; the wol mutant has increased numbers of protoxylem cell files and loss of other cell types in the root vasculature Caño-Delgado et al. (2000), Mähönen et al. (2000), Scheres et al. (1995) ARABIDOPSIS HISTIDINE PHOSPHOTRANSFER PROTEIN 6 (AHP6) Cytokinin signaling inhibitor Restricts the domain of cytokinin activity by allowing protoxylem differentiation in a spatially specific manner Mähönen et al. (2006a) PIN1 Auxin-efflux carrier PIN1 is expressed in vascular tissues; a pin1 mutant impairs vein pattern formation, producing ectopic differentiated veins in leaves and additional vascular bundles in shoots; pin1 phenotypes are similar to NPA treatments Galweiler et al. 1998, Ibañes et al. 2009, Mattsson et al. (1999, 2003), Wenzel et al. (2008) TF, transcription factor; LRR, leucine-rich repeat. walls. By contrast, xylem vessel precursors in the inner layers differentiate into metaxylem with reticulate or annular secondary cell walls. This xylem patterning in the Arabidopsis root is regulated by both transcriptional and posttranscriptional regulations that are mediated by GRAS (GAI, RGA, SCR) family TFs, SHORT ROOT (SHR) and SCARECROW (SCR), and five class III homeodomain-leucine zipper (HD-ZIP III) TFs (Carlsbecker et al. 2010). SHR proteins, produced in the vascular cylinder, move into the endodermis layer and activate the expression of SCR (Helariutta et al. 2000, Levesque et al. 2006, Nakajima et al. 2001). These two TFs form complexes and activate two genes encoding microRNA (miR) 165/166 in the endodermis layer. Subsequently, miR 165/166 diffuses out of the endodermis and 610 Caño-Delgado · · Lee Demura leads the degradation of mRNAs of HD-ZIP III TFs in the periphery of the vascular cylinder. In the absence of miR-mediated mRNA degradation, protoxylem in the xylem periphery is replaced by metaxylem owing to a high level of HD-ZIP III TFs throughout the xylem axis. In addition to specifying metaxylem cell fate with their high dosages, HD-ZIP III TFs drive the de novo xylem formation. As multiple HD-ZIP III TFs are knocked out, the metaxylem in the center of the xylem axis is replaced by the protoxylem. When all five HD-ZIP III TFs are knocked out, xylem formation is no longer detected in the root (Carlsbecker et al. 2010). The development of phloem in the root meristem starts with the asymmetric cell division of phloem initials, which forms phloem sieve cells and companion cells. ALTERED Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. CB26CH24-Cano-Delgado ARI 3 September 2010 20:17 PHLOEM DEVELOPMENT (APL), a myb family TF, promotes the asymmetric cell division of a phloem initial in Arabidopsis roots (Bonke et al. 2003). Interestingly, in apl mutants the phloem initial cell not only fails to undergo asymmetric cell division but also turns into ectopic xylem. When APL is ectopically expressed, differentiation of xylem precursors is suppressed. These observations suggest that, in addition to promoting asymmetric cell division for phloem formation, APL regulates signaling processes that suppress xylem differentiation. Xylems and phloems always develop in parallel along the boundaries of procambium/ cambium, the vascular stem cells. Recent studies suggest that the procambium/cambium mediates the signaling that sets up the boundaries between xylem and phloem. This signaling is regulated by CLAVATA3 (CLV3)-like small protein ligands (CLEs) and their receptor-like protein kinase. CLE 41/44 secreted from the phloem bind to CLV1-like leucine rich repeat (LRR) receptor-like kinase (RLK), PXY (PHLOEM INTERCALATED WITH XYLEM), which is specifically expressed in the procambium/cambium (Fisher & Turner 2007). This interaction is important for regulating cell division activity in the procambium/cambium and for balancing the pluripotent procambial/cambial cells and differentiating xylem and phloem (Etchells & Turner 2010, Hirakawa et al. 2008, Whitford et al. 2008). Ectopic expression studies of CLE41 and PXY suggested that a higher dosage of CLE41 than PXY promotes cell division but inhibits xylem cell differentiation, whereas equal dosages of CLE41 and PXY balance cell division and xylem differentiation. However, the cell proliferation activity of CLE41 requires PXY; in a pxy mutant, cell proliferation by ectopic CLE41 expression was suppressed (Etchells & Turner 2010). Unlike vascular tissues in the root, which are organized in a cylindrical structure, those in stems are arranged collaterally (Figure 2) or bicollaterally. For vascular tissues in the shoot to connect to those in the root, the reorganization of the xylem and phloem strands should happen in the transition zone between the shoot and the root. Anatomical characterization showed that xylem and phloem strands in the root vascular cylinder bifurcate in the hypocotyl area to reorganize in stems and leaves (Busse & Evert 1999b). In stems and leaves with collateral vascular bundles, xylem is specified in the adaxial (toward the meristem) and phloem in the abaxial (away from the meristem) regions. In stems and leaves with bicollateral vascular bundles, phloem forms both inside and outside the xylem. Collateral vascular patterning is disrupted when miR 165/166 fails to suppress HD-ZIP III TFs (Emery et al. 2003, Itoh et al. 2008, Zhong & Ye 2004). Dominant gain-of-function mutants of REVOLUTA (REV) in Arabidopsis and ectopic expression of miR-resistant HD-ZIP III TFs in rice result in the formation of amphivasal vascular bundles (xylem surrounds phloem) in stems and leaves. However, the loss of three closely related HD-ZIP III TFs PHABULOSA (PHB), PHAVOLUTA (PHV), and REV in Arabidopsis results in amphicribal vascular bundles (phloem surrounds xylem). Regulators of vascular patterning in stems and leaves are also involved in the determination of the polarity of lateral organs (Husbands et al. 2009). Mutations causing amphivasal bundles result in leaves that are radialized with adaxial surface features throughout. Conversely, those causing amphicribal bundles result in abaxialized leaves (Emery et al. 2003). An answer to how gene regulatory programs involved in vascular patterning are related to the polarity of lateral organs could emerge with a more thorough understanding of the underlying molecular mechanisms in each developmental process. A genetic study showed that the regulation of vascular bundle densities is also important for the plant growth and development. The stems of cov1 (continuous vascular ring) (Parker et al. 2003) and hca (high cambial activity) (Pineau et al. 2005) mutants develop a higher density of vascular bundles and promote more cambium development than do wild-type stems. The COV1 gene encodes a membrane-localized www.annualreviews.org • Plant Vascular Patterning LRR: leucine-rich repeat RLK: receptor-like kinase Vascular bundle: a discrete strand of xylem and phloem cells separated by procambium 611 CB26CH24-Cano-Delgado ARI 3 September 2010 20:17 protein whose molecular function is yet to be discovered. SAM: shoot apical meristem Vascular Tissue Formation During Plant Growth: Venation Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. PAT: polar auxin transport Secondary growth: the radial growth of stems and roots driven by cell division from the cambium; the meristem that is established postembryonically 612 As plants grow apically, lateral organs continuously develop from the shoot apical meristem (SAM). As lateral organs emerge, vascular tissues grow toward organ primordia and branch in apical and lateral directions to form veins, the networks of vascular bundles. Temporal and spatial organizations of veins are diverse and unique to plant lineages, but, in a broad sense, veins are reticulate in dicots and striate in monocots. The highly ordered vein growth patterns (Nelson & Dengler 1997) suggest the presence of positional information that spatially and temporally regulates vein growth. Theoretical studies suggested that the positional information that emerges from the organ primordia canalizes into the subset of cells of future veins. Experimental studies on auxin distribution and signaling suggested that auxin might be the positional information (Sachs & Woolhouse 1981). The auxin efflux carrier, PIN-FORMED1 (PIN1), visually supports this auxin canalization theory. Auxin induces PIN1 expression, and PIN1 proteins are localized in the basal region of the cells from which auxin flows. PIN1 is also expressed in the cells that will become the vascular strand (Galweiler et al. 1998). Its expression domains were shown to acropetally expand through the future veins as leaf primordia emerged and grew (Scarpella et al. 2006). When the veins were about to bifurcate, PIN1 localization in the bifurcating cell became bipolar. This further supports the hypothesis that auxin flow directs vascular tissue specification. PIN proteins cycle between plasma membranes and endosomes via the activity of an ADP ribosylation factor–guanyl nucleotide exchange factor (ARF-GEF), GNOM (GN) (Geldner et al. 2003). The importance of polar auxin transport (PAT) in vein growth and patterning was further supported by the finding that mutations in components of auxin Caño-Delgado · · Lee Demura transport resulted in abnormal vein patterning. One mutant, scarface (sfc) or van3, generates dense but fragmented vein islands on leaves and cotyledons. This phenotype is caused by the mutation of a gene encoding ADP ribosylation factor GTPase activating protein (ARF-GAP) (Deyholos et al. 2000, Koizumi et al. 2005, Sieburth et al. 2006), a modulator of ARF-GEF involved in vesicle trafficking. SFC/VAN3, localized in the transGolgi network, interacts with COTYLEDON VASCULAR PATTERN 2 (CVP2), which encodes inositol polyphosphate 5 -phosphatases (Carland & Nelson 2004). The phosphatidyl inositol-4-phosphate generated by CVP2 acts as a ligand of SFC/VAN3 and its interactor VAB (VAN3 binding protein) and then modulates the ARF-GAP activity of SFC/VAN3 (Carland & Nelson 2009, Naramoto et al. 2009). In the absence of ARF-GEF activities, PIN1 failed to localize properly in response to polar auxin transport (Sieburth et al. 2006). For cells through which auxin is canalized to be specified into vascular cell precursors, specific transcriptional regulation should be initiated. A recent study suggests that one of the earliest responsive transcriptional regulators of auxin is HD-ZIP III TF ATHB-8 (ARABIDOPSIS THALIANA HOMEOBOX PROTEIN-8) (Donner et al. 2009). ATHB-8 is directly activated by MP. ATHB-8 subsequently directs the formation of preprocambial cells and further induces the expression of PIN1, which was also shown to be auxin responsive (Scarpella et al. 2006). Vascular Tissue Formation During Plant Growth: Secondary Growth Most vascular plants grow in both apical and radial directions. The radial growth, or secondary growth, in stems and roots is promoted by the active proliferation of vascular cells in the cambium. Although cell division activities in the cambium are most pronounced in perennial tree species, they also occur in herbaceous plants. The only exceptional case is monocots. Unlike in other flowering plants Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. CB26CH24-Cano-Delgado ARI 3 September 2010 20:17 and gymnosperms, in monocots the cambium does not develop likely because of the loss of cambium formation capabilities before their divergence. In the root, the cambium is derived from the procambium and the pericycle on the xylem axis (Baum et al. 2002, Sundberg 1983). In the stem, the procambium in the vascular bundle (called fascicular cambium) and cells between the vascular bundles (interfascicular cambium) together form the cambium (Esau 1977). Of daughter cells generated in the cambium, only those located farther from the cambium differentiate into vascular cells; cells located in the center of stems and roots differentiate into xylem, and cells located in the periphery of stems and roots differentiate into phloem (Figure 2). This asymmetric cell division and differentiation helps maintain the pluripotent stem cell population in the cambium and the polar organization of xylem and phloem. Cambial activities heavily depend on temperature, light, and resource availability, and likely integrate many internal and external signals. Mutant screening in Arabidopsis identified that cov1 (Parker et al. 2003) and hca (Pineau et al. 2005) mutants that develop vascular bundles in a higher density also have higher cambium activities. Distinct from COV1 and HCA, PXY seems to be involved in the spatial patterning of vascular tissues. Unlike in the wild type, in a pxy mutant, phloem and xylem do not differentiate in a polar manner, which results in an unclear boundary between phloem and xylem (Fisher & Turner 2007). As described above, this gene, which encodes an LRR RLK similar to CLV1, is also involved in the spatial patterning of xylem and phloem in the procambium of roots and stems, which suggests overlapping regulatory programs in the stem cells for primary and secondary vascular tissue development. Recent genome-wide gene expression profiling in the cambial zone of Arabidopsis and Populus has started to reveal more genes involved in secondary growth (Schrader et al. 2004b, Zhao et al. 2005). Expression profiling in the cambial zone in Populus suggested that SAM and cambium may share a partially overlapping molecular mechanism. In SAM, CLV and WUSCHEL (WUS) form a feedback loop that balances an undifferentiated stem cell population with cells that will differentiate (Dodsworth 2009). Independently of the WUS-CLV pathway, SHOOT MERISTEMLESS (STM) plays important roles in maintaining stem cells in SAM (Long et al. 1996). Interestingly, the two genes most closely related to CLV1 in Populus were found to be induced in the xylem and phloem sides of cambium, respectively. Furthermore, WUSlike genes and CLEs were also highly induced in the cambial zone. A recent finding of expression and promotion of stem cell division of WUSCHEL-related HOMEOBOX 4 (WOX4) in the procambium/cambium of Arabidopsis and tomato further support the conserved mechanism of the WUS-CLV pathway in the SAM and vascular stem cells ( Ji et al. 2010). Putative orthologous genes of STM and its indirect downstream regulator BREVIPEDICELLUS (BP) in Populus, ARBORKNOX1 and 2, were also highly induced in the cambial zone (Du et al. 2009, Groover et al. 2006). Functional analyses of ARBORKNOX1 and 2 suggested that these genes repress the differentiation of vascular tissues, by which they likely maintain the stem cell population in the cambial zone. Many perennial trees living in areas with distinctive seasons undergo reprogramming of meristem activities as the seasons change. Comparison of gene expression profiles in dormant and active cambium showed dramatic changes in overall gene expression. In particular, many genes involved in meristem activities and cell cycle regulation were found to be downregulated. By contrast, genes involved in stress responses and dormancy were upregulated (Schrader et al. 2004a). Vascular Cell Type Specification and Gene Expression Genetic screening in model species has identified several key regulators in the specification and patterning of vascular cell types. www.annualreviews.org • Plant Vascular Patterning 613 CB26CH24-Cano-Delgado ARI Transdifferentiation: differentiation of already differentiated cells with distinct functions into different cell types Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. FACS: fluorescenceactivated cell sorter 614 3 September 2010 20:17 However, approaches that rely only on forward genetics to identify the connectivity among the regulators and their downstream genes have been difficult because visualizing vascular tissue phenotypes in stems and roots requires several histological procedures. In recent years, genome sequencing of several vascular plants, advancement in high-throughput technologies for gene expression profiling, and development of tools for targeted gene expression perturbation have dramatically shifted the direction of research. Large-scale gene expression profiling using various perturbation approaches has yielded information about genes that are expressed in vascular cell types and their dynamic changes during vascular cell specification and differentiation that has allowed for the identification of regulators involved in vascular tissue development. Gene expression dynamics in xylem are particularly interesting because many changes occur during its specification and differentiation. In Zinnia and Arabidopsis, leaf mesophyll cells or subcultured suspension cells can be induced to transdifferentiate into xylem cells in the cell culture systems. Using this in vitro culture system, global gene expression changes during transdifferentiation were identified (Demura et al. 2002, Kubo et al. 2005). These global gene expression profiles revealed gene sets that are induced in a specific stage of transdifferentiation. Noticeably, seven NAC (NO APICAL MERISTEM, ATAF1, ATAF2, and CUC2) domain TFs were induced during xylem differentiation in Arabidopsis and Zinnia; these were therefore named VASCULARRELATED NAC-DOMAIN PROTEINs (VNDs). Among them, ectopic expression of VND6 in Arabidopsis triggered ectopic metaxylem formation. By contrast, ectopic VND7 resulted in ectopic protoxylem formation. However, their knockout mutant did not show any phenotype, suggesting the presence of genetic redundancy. These studies demonstrate that well-designed large-scale gene expression experiments can successfully identify regulators that are unlikely to be revealed otherwise. Caño-Delgado · · Lee Demura During plant development, neighboring cell types specify and differentiate together. Therefore, it is important to understand how gene expression for the specification and differentiation of cell types of interest is regulated in the context of neighboring cell types and the organs they inhabit. High-resolution transcriptome data at the cell type level can serve as resources for addressing such questions and those regarding further regulatory networks (Lee et al. 2005). In Arabidopsis root, transcriptome profiling of all major cell types has been completed using cell sorting–microarray technology (Birnbaum et al. 2003, 2005; Brady et al. 2007; Lee et al. 2006; Nawy et al. 2005), which tags the cell type with fluorescent markers (described in more detail below). Specifically, roots expressing cell type–specific fluorescent markers are digested with cell wall–digesting enzymes to generate protoplasts. Fluorescent protoplasts are isolated with a fluorescenceactivated cell sorter (FACS), and their RNA is isolated, amplified, and labeled for hybridization to microarrays. Using this method, 19 cell type–specific expression datasets were generated. These include two xylem datasets (early xylem precursors, differentiating xylem) and three phloem datasets (protophloem sieve cells, phloem sieve cells and companion cells, mature companion cells). A search for cell type–enriched genes in these 19 datasets showed the highest number of enriched genes in xylem. Among them, genes enriched in early xylem were found to be involved in translation initiation and elongation, RNA binding and processing, and mitosis. In differentiating xylem, genes involved in secondary cell wall biosynthesis were most significantly enriched (Brady et al. 2007). Based on the root expression atlas, cell type–specific expression of representative transcriptional regulators was validated by generating transgenic lines expressing green fluorescent protein (GFP) under 5 upstream intergenic regions of transcriptional regulators (Table 2). Comparing their expression patterns with root expression data using an unbiased image analysis suggested that the cell sorting–based root expression atlas CB26CH24-Cano-Delgado Table 2 ARI 3 September 2010 20:17 Summary of vascular cell type markers available Reporter Marked cells Description Reference Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. Provascular pWOL-GFP Stele Root stele at the root meristem and starts to fade from elongation zone Mähönen et al. (2000), Birnbaum et al. (2003) pATHB-8-GUS Provascular cells Provascular cells in the root meristem and at the hipocotyl, leaves, and stems (see Figure 3) Baima et al. (1995), Scarpella et al. (2004, 2006) pATHB-15-GUS Provascular cells Provascular cells in the root and vascular bundles of inflorescence stems Ohashi-Ito & Fukuda (2003), Fisher & Turner (2007) pPXY-GUS Procambial cells Provascular tissues in the inflorescence vascular bundles Fisher & Turner (2007), Hirakawa et al. (2008) pBRL1-GUS Procambial, phloem, and phloem-pericycle cells Spatial distribution in the provascular and phloem cells at the stem vascular bundles Caño-Delgado et al. (2004) pBRL3-GUS Stele, procambial cells differentiating into xylem Provascular cells from the elongation zone of the root; provascular tissues in the inflorescence stem Caño-Delgado et al. (2004) A8 (pAT3G48100-GFP) Procambial cells GFP in the lateral root cap and stele procambium of the root meristem Lee et al. (2006) pAHP6-GFP Protoxylem and adjacent pericycle cells Primary root Mähönen et al. (2006a) pVND6-YFPnls Differentiating metaxylem Tracheary element differentiation expressed in roots Kubo et al. (2005) pVND7-YFPnls Differentiating protoxylem Tracheary element differentiation expressed in roots Kubo et al. (2005) ProASL19:EGFP-GUS Differentiating xylem Primary root Soyano et al. (2008) ProASL20:EGFP-GUS Differentiating xylem Primary root Soyano et al. (2008) pXCP2:GUS Xylem Xylem cell death Funk et al. (2002) pACL5-GUS Xylem Xylem differentiation in root, hypocotyls, and shoots Muñiz et al. (2008) S18 (pAT5G12870-GFP) Maturing xylem cells Starts from mid-elongation and stops halfway; GFP switches from protoxylem to metaxylem Lee et al. (2006) S4 (pAT3G25710-GFP) Xylem Very weak GFP from xylem precursors in the root meristem Lee et al. (2006) J2501 Pericycle, protoxylem, metaxylem, phloem Characterized in the primary root J1721 Protoxylem, collumela Strong labeling in the primary root; also associated expression in the QC and columella cells (see Figure 3) S22 (pAT4G28140-GFP) Xylem GFP in xylem from meristematic to early maturation zones of the root Lee et al. (2006) S20 (pAT1G71930-GFP) Xylem GFP in the xylem of elongation and the maturation zone of the root Lee et al. (2006) Xylem pXYN3-YFPnls (Continued ) www.annualreviews.org • Plant Vascular Patterning 615 CB26CH24-Cano-Delgado Table 2 ARI 3 September 2010 20:17 (Continued ) Reporter Marked cells Description Reference proAPL-GUS; proAPL-GFP Developing pSE and mSE and CC: loss of GFP in mature pSE is accompanied by strong GFP in neighboring CC; GFP reappears in immature mSE From mid-meristematic zone to top. Strong at the start, then fades, then become stronger when root hair becomes mature length Bonke et al. (2003) S32 (pAT2G18380-GFP) Phloem sieve cells Root protophloem and metaphloem sieve cells from the vascular initials to top Lee et al. (2006) SUC2 Companion cells Companion cells starting from elongation; GFP is stronger when root hair is obvious (2 mm from tip) Imlau et al. (1999) pPP2–2 A-YFPnls Phloem Companion cells in the elongation zone of the root (see Figure 3) PD markers Phloem PD1 to PD6 report GUS expression in distinct phloem domains at different developmental stages Bauby et al. (2007) S29 (pAT2G37590-GFP) Phloem precursor GFP in the phloem precursors of the root meristem Lee et al. (2006) Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. Phloem GFP, green fluorescent protein; YFPnls, nuclear-localized yellow fluorescent protein; QC, quiescent center; GUS, β-glucuronidase. well represents the in vivo expression patterns of the genes (Lee et al. 2006, Mace et al. 2006). Vascular development in monocots is understudied in comparison with eudicots. Recently, the gene expression atlas for the major tissues and organs of rice, including vascular tissues, was generated using the laser capture microdissection technique ( Jiao et al. 2009, Nelson et al. 2006). Among the 1,126 rice genes identified as orthologs of genes in Arabidopsis, 112 were more than twofold enriched in vascular tissue compared with the cortex. Furthermore, 77 of the 112 were also enriched under the same criteria using Arabidopsis root expression data ( Jiao et al. 2009). This suggests significant conservation of expression patterns in the vascular tissues of evolutionarily divergent plants. BR: brassinosteroid TE: tracheary element HORMONAL REGULATION OF VASCULAR TISSUE/CELL SPECIFICATION Plant hormones play essential roles in the control of vascular development. An increasing 616 Caño-Delgado · · Lee Demura number of studies, mostly carried out in the model systems Arabidopsis, Zinnia, and Populus, have shown that the plant hormones auxin, brassinosteroid (BR), and cytokinin, among others, play unique and interconnected roles during distinct vascular development events. The Roles of Auxin in Vascular Cell Differentiation Indole-3-acetic acid (IAA, the predominant auxin in higher plants) is essential for vascular tissue development. It promotes cambial cell divisions (Schrader et al. 2004a, Ye 2002, Ye & Varner 1994), induces the differentiation of xylem tracheary elements (TEs) (Aloni 1987; Fosket & Torrey 1969; Fukuda 1997, 2004; Fukuda & Komamine 1980; Sachs & Woolhouse 1981; Yoshida et al. 2009), and contributes to the maintenance of vascular continuity along different plant organs (Berleth et al. 2000, Hardtke & Berleth 1998, Scarpella et al. 2006). Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. CB26CH24-Cano-Delgado ARI 3 September 2010 20:17 A variety of approaches, including classical physiology, genetics, and transcriptomics, have contributed to substantially advancing our understanding of the role of auxin signaling, responsiveness, and transport in plant vascular development. It is well established that IAA application can define the sites of vascular cell differentiation. Initial physiological studies into sterile-cultured stem pith sections of tobacco (Nicotiana tabacum) (Clutter 1960) and soybean (Glycine max) callus (Fosket & Torrey 1969), as well as later research using the mesophyll cell culture system from Zinnia, demonstrated that exogenous auxin application triggers xylem TE differentiation (Fukuda & Komamine 1980). Further supporting this idea, the application of 1-N-naphthylphthalamic acid (NPA), the inhibitor of PAT, prevents TE differentiation. Molecular studies using Zinnia as a model system identified several auxin signaling and transport genes that participate in TE differentiation [homologs of Arabidopsis Aux/IAA, auxin response factors (ARFs), and auxin influx and efflux carriers] (Demura et al. 2002, Milioni et al. 2001, Yoshida et al. 2009). However, the precise mechanism by which increasing auxin levels can trigger the differentiation of xylem cells remains to be identified. Studies of secondary growth in tree species have shown that the highest levels of auxin are found in the cambium of Pinus and Populus, consistent with a role for auxin in maintaining cambial cell identity (Uggla et al. 1996, 1998). In Pinus, auxin concentrations determined by fine gas chromatography–mass spectrometry techniques were found to peak at the cambial meristematic cells. The endogenous auxin levels measured in tree species confirmed mathematical predictions for a correlation between changes in cambial cell polarity and auxin gradient distribution in those cells (Kramer et al. 2008). A transcriptional study from cambial meristematic cells in poplar demonstrated that increased auxin levels in those cells positively correlate with the upregulation of cell cycle– related genes (Schrader et al. 2004b). Beyond the physiological and transcriptomics experiments, in-depth characterization of Arabidopsis mutants has been fundamental for understanding how auxin signaling mediates vascular development (see the section on venation above). Genetic approaches permitted the identification of YUCCA (Yucca1) family members that encode a flavin monooxygenaselike enzyme involved in auxin biosynthesis in Arabidopsis (Cheng et al. 2006, Zhao et al. 2001). Although Yucca gain-of-function mutants have an ∼50% increase in free auxin compared with wild-type plants, these plants do not exhibit an increased number of shoot vascular bundles compared with the wild type (Ibañes et al. 2009). Conversely, double and triple lossof-function mutants yuc1yuc4 and yuc1yuc2yuc4 have simplified leaf venation patterns (Cheng et al. 2006). Based on these findings, auxin distribution rather than auxin level was proposed to drive vascular patterning, although a minimum threshold of local auxin levels may be required to initiate vascular strand formation. NPA: 1-Nnaphthylphthalamic acid Auxin Transport in Vascular Patterning PAT is required for the formation of a continuous vascular strand. A series of physiological experiments have demonstrated that local application of IAA induces vascular strand formation, and a new functional vein will extend basally from locally applied IAA (Aloni 1987, Fukuda 2004, Sachs & Woolhouse 1981, Sauer et al. 2006, Sieburth & Deyholos 2006, Ye 2002). Auxin is synthesized in the shoot apex and transported via a unique mechanism that is central to axis formation and patterning in plants (for recent reviews, see Petrasek & Friml 2009, Smith & Bayer 2009, Vanneste & Friml 2009). The directionality of this transcellular transport depends on gradients of auxin influx and efflux carriers that continuously cycle between plasma membrane and intracellular compartments (Kramer 2004, 2009). The polar localization of auxin carriers in the plasma membrane determines the directionality of the flow. Thus, PAT generates auxin maxima and gradients within tissues that are instrumental in the regulation of various developmental www.annualreviews.org • Plant Vascular Patterning 617 CB26CH24-Cano-Delgado ARI 3 September 2010 20:17 processes, including vascular tissue formation (Smith & Bayer 2009). Recent studies have shown that auxin controls PIN1 protein localization, which is likely to provide a positive feedback loop for the formation of vascular strands (Scarpella et al. 2006), thus refining the original prediction of the auxin flow canalization hypothesis (Sachs & Woolhouse 1981). Auxin efflux carriers belong to PIN family members of transmembrane proteins that are asymmetrically distributed at the basal end of PAT-competent cells (for a recent review see Petrasek & Friml 2009). An appropriate asymmetric localization of efflux carriers is needed to elicit auxin maxima at the position of vascular bundles in the shoot of Arabidopsis (Galweiler et al. 1998, Ibañes et al. 2009). Auxin transport inhibition by NPA treatment or pin1 mutations impairs vein pattern formation producing ectopic differentiated veins in leaves and additional vascular bundles in shoots (Ibañes et al. 2009; Mattsson et al. 1999, 2003; Wenzel et al. 2008) (Figure 3). It has been shown that NPA blocks PIN1 cycling (Geldner et al. 2001), and the phenotypes of NPA-treated plants are similar to those of pin1 mutants (Berleth et al. 2000; Mattsson et al. 1999, 2003; Okada et al. 1991; Sieburth & Deyholos 2006; Wenzel et al. 2008). Despite the evidence showing that auxin influx carrier AUX1/LAX family members impact plant gravitropism (Bennett et al. 1996, Marchant et al. 1999, Swarup et al. 2005), lateral root initiation (Swarup et al. 2001, 2008), and phyllotaxy (Bainbridge et al. 2008, Bayer Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. BL: brassinolide et al. 2009), their effects in vascular patterning if any, await to be studied. Brassinosteroid Signaling During Vascular Development To date, most of the knowledge concerning the role of steroid hormone BRs in vascular development has been contributed by physiological studies in Zinnia and Arabidopsis. Brassinosteroid studies in Zinnia. BRs act at later stages to promote TE differentiation in Zinnia xylogenic cell cultures (Fukuda 1997, Yamamoto et al. 1997). In these cultures, the levels of BR intermediates peak at the transition from undifferentiated cells to TEs (Yamamoto et al. 2001). Moreover, the BR synthesis inhibitors uniconazole and brassinazole prevent xylem differentiation (Asami et al. 2000), which can be restored by exogenous application of BR. Notably, BR biosynthetic enzymes ZeDWF4 and ZeCPD1 appear to be expressed in differentiating procambial and xylem cells (Yamamoto et al. 2007). It has been shown that BRs regulate the differentiation from procambium to xylem through specific members of the ZeHD-ZIP III family (Fukuda 2004, OhashiIto & Fukuda 2003, Ohashi-Ito et al. 2002). The expression of ZeHB-12 is induced by exogenous brassinolide (BL) application, whereas the inducible expression of the ZeHB-12 transcript in Arabidopsis was shown to promote the −−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→ Figure 3 Modeling vascular patterning at the shoot inflorescence stem of Arabidopsis. (a) Primary vascular bundle (VB) pattern scheme: procambium ( yellow), protoxylem (light blue), xylem and interfascicular fibers (IFs) (dark blue), and phloem (orange). (b) Auxin maxima (blue), driven by polar transport ( gray arrows, plotted outside cells for clarity), position VBs along the vascular ring of cells (black boxes). (c) Numerical simulation results for auxin concentration ([Auxin]) in arbitrary units along a ring of NF = 210 final cells arising from an initial pool of Ni = 120 progenitor cells; x and y stand for spatial coordinates (wild-type average diameter used). (e, g) Simulation results for the auxin concentration along a ring of a few (e) and many ( g) cells, mimicking brassinosteroid (BR)-loss- and gain-of-function mutants, respectively. Parameter values as in (c) with (e) Ni = 80, NF = 100 and ( g) Ni = 135, NF = 250 cells. These figures are from Ibañes et al. (2009) and are reproduced with permission of the Proceedings of the National Academy of Sciences, USA. Vascular defects in the VBs of BR mutants are shown by comparing a cross section at the base of the inflorescence of a wild-type Col-0 plant (d ), a mutant with reduced BR signaling, bri1-116 ( f ), and a mutant with enhanced BR signaling, bes1-D (h). 618 Caño-Delgado · · Lee Demura CB26CH24-Cano-Delgado ARI 3 September 2010 20:17 a b [Auxin] (arb. units) d 6 5 4 3 2 1 0 6 c 4 2 0 4 400 200 –400 –200 [Auxin] (arb. units) x (μm) 6 5 4 3 2 1 0 0 200 0 y (μm) –200 –400 400 500 μm 6 e 4 2 f 0 –400 –200 0 x (μm) 200 –400 400 –200 0 200 400 y (μm) 200 μm h [Auxin] (arb. units) Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. Auxin maxima 6 5 4 3 2 1 0 6 g 4 2 0 400 200 –400 –200 0 x (μm) 200 400 0 y (μm) –200 –400 500 μm www.annualreviews.org • Plant Vascular Patterning 619 CB26CH24-Cano-Delgado a ARI 3 September 2010 b BRI1-like members 20:17 BRL2/VH1 BL OH OH C ID C HO C O At4g39400 At1g55610 At3g13380 HO Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. O c ID At4g39400 d SERK3/BAK1-like C PXY/CLV1-like CLE41/44 At5g61480 At1g08590 At4g28650 At1g71830 At4g30520 Figure 4 Leucine-rich repeat (LRR)-receptor proteins involved in vascular development. To date only a few LRR receptor-like kinase proteins have been related to plant vascular development. Interestingly, LRR-receptor signaling during vascular development can be triggered by binding of protein (CLE41/44) and nonprotein [brassinolide (BL)] ligands, which are perceived by the PXY receptor and the BR-INSENSITIVE 1 (BRI1)-family of LRR-receptors, respectively. (a,b) Schematic representation of BRI1 family members, BRI1, BRL1, and BRL3 (encoded by At4g39400, At1g55610, and At3g13380, respectively), which bind to BL via the extracellular LRR and the 70-amino acid island domain (ID) (Caño-Delgado et al. 2004, Kinoshita et al. 2005). To date, the ligand for provascular specific receptor BRL2/VH1 (At2g01950) is not known. The SERK1 (SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE 1) receptor (encoded by At1g71830) is expressed in the root vasculature (Kwaaitaal & de Vries 2007), and a homolog of SERK3/BAK1-like protein (encoded by At4g30520) is induced by ZeHD12 in the vasculature (Ohashi-Ito et al. 2005). (c,d ) PXY (encoded by At5g61480) is specifically involved in vascular bundle polarity (Fisher & Turner 2007), and photoaffinity labeling experiments showed that CLE41/CLE44 peptides bind to the PXY receptor (Hirakawa et al. 2008). Two closely related LRR-kinase proteins (encoded by At1g08590 and At4g28650) named PXY-LIKE (PXL1 and PXL2, respectively) have been proposed to function redundantly with PXY in vascular development. 620 Caño-Delgado · · Lee Demura expression of BRL3 (BRASSINOSTEROID RECEPTOR LIKE 3) and a BAK1/SERK3like (BRI1 ASSOCIATED RECEPTOR KINASE 1/SOMATIC EMBRYOGENESIS RECEPTOR KINASE 3) gene (At4g30520) in the shoot vasculature (Ohashi-Ito et al. 2005; Figure 4). On this basis, it has been proposed that BRL3 together with BAK1/SERK3-like receptors (At4g30520) may mediate xylemspecific BR signaling events downstream of ZeHB-12, but the potential gene regulatory loops connecting BR signaling to Class III homeodomain family members are yet to be characterized. Brassinosteroid signaling during vascular development in Arabidopsis. BRs have been shown to play important roles in promoting cell expansion and vascular development in several plant species (Vert & Chory 2006). Unlike their animal counterparts, BRs in plants are perceived at the plasma membrane by direct binding with BRI1 (BR-INSENSITIVE 1) (Kinoshita et al. 2005, Wang et al. 2001), a LRR-RLK protein that acts in concert with BAK1/SERK3, a related LRR-RLK, to transduce BR signals into the cytoplasm (Li et al. 2002, Russinova et al. 2004). The downstream signaling events of the BRI1 receptor are among the best-characterized signaling pathways in plants. In addition to the BRI1 receptor, two BRI1-homolog proteins, BRL1 and the BRL3 (BRASSINOSTEROID RECEPTOR LIKE 1 and 3, respectively), have been identified as binding BRs with high affinity (CañoDelgado et al. 2004, Kinoshita et al. 2005). These receptors are predominantly expressed in provascular tissues. Based on the phenotypes of double- and triple-mutant combinations, BRI1 family members were proposed to function redundantly in the elaboration of xylem: phloem differentiation ratios at the vascular bundles of the shoot inflorescence stem. In addition to BRI1, BRL1, and BRL3, the LRR-receptor kinase protein VH1 (VASCULAR HIGHWAY 1)/BRL2 was identified as expressed in the procambium and required for normal phloem function (Clay Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. CB26CH24-Cano-Delgado ARI 3 September 2010 20:17 & Nelson 2002). VH1/BRL2 belongs to the BRI1-like family, each member of which is characterized by the presence of a 70-amino acid island domain (ID) that interrupts the extracellular LRRs (Caño-Delgado et al. 2004, Clay & Nelson 2002, Li & Chory 1997; Figure 4). Although the ID is required for BL binding (Kinoshita et al. 2005, Wang et al. 2001), the VH1/BRL2 receptor was not able to bind BL with high affinity; neither did complementary bri1 mutant phenotypes when expressed under the control of a BRI1 promoter. A recent search for VH1/BRL2 interactive proteins identified a tetratricopeptide repeat (TPR)-containing protein, VIT (VH1-interacting TPR-containing protein), and a MAP kinase kinase kinase, VIK (VH1interacting kinase), that function in initial and later stages of vascular strand formation, respectively (Ceserani et al. 2009). Together, the characterization of these four BRI1-like receptors offers an excellent example of functional diversity in RLK subfamilies in Arabidopsis. Among the more than 200 annotated LRR-RLK proteins in Arabidopsis, only the signaling triggered by BL, a nonprotein ligand that binds BRI1, BRL1, and BRL3 receptors (Caño-Delgado et al. 2004, Clay & Nelson 2002, Kinoshita et al. 2005, Li & Chory 1997, Wang et al. 2001), and the PXY-like family of receptors that binds to CLE41/44 peptides, have been reported to function in vascular development (Hirakawa et al. 2008, Whitford et al. 2008; Figure 4). Meanwhile, the nature of the ligand triggering VH1/BRL2 response in vascular development is yet to be discovered. Initial evidence for a role for BRs in Arabidopsis vascular development comes from the characterization of BR-deficient mutants cpd and dwf7 (Choe et al. 2001, Szekeres et al. 1996) and perception mutants (Caño-Delgado et al. 2004). A recent comprehensive analysis of BR mutants has permitted researchers to consider a role for BRs in promoting vascular bundle formation (Ibañes et al. 2009; Figure 3). Mutants with reduced BRI1 receptor activity, signaling, or levels (Li & Chory 1997, Szekeres et al. 1996) were found to have a reduced number of vascular bundles and auxin maxima, whereas mutants with increased BR signaling (Wang et al. 2002, Yin et al. 2002) or levels (Choe et al. 2001) exhibited an increased number of vascular bundles. This study proposes that BR signaling promotes procambial cell division during the elaboration of the vascular pattern. The roles of BRs in cell proliferation have remained controversial to date (Clouse et al. 1996, Miyazawa et al. 2003); future experiments to determine whether BRs primarily control the meristematic function of procambial cells are needed. Cytokinins During Vascular Cell Differentiation Physiological experiments in Zinnia xylogenic cultures have shown that the hormone cytokinin in conjunction with auxin promotes the differentiation of TEs (Aloni 1987, Fukuda 1997, Fukuda & Komamine 1980). Based on the recent characterization of cytokinin signaling components in poplar stems, cytokinins have been shown to contribute to the maintenance and proliferation of cambial cells in tree species (Matsumoto-Kitano et al. 2008, Nieminen et al. 2008). Transgenic trees expressing a cytokinin catabolic gene from Arabidopsis (CYTOKININ OXIDASE 2) exhibit reduced cambial activity that correlates with a reduction in radial plant growth, indicating that cytokinin promotes cambial cell divisions. In Arabidopsis, elegant genetic studies have shown the importance of cytokinin in several aspects of vascular development, including proliferation, patterning, and differentiation of distinct vascular cells types (reviewed in Elo et al. 2009, Mähönen et al. 2006b). The wooden leg (wol ) mutant allele exhibits an increased number of protoxylem cell files and loss of other cell types in the root vasculature (CañoDelgado et al. 2000, Mähönen et al. 2000, Scheres et al. 1995). The wol mutant has a point mutation (T278I) in the WOL/CRE1/AHK4 histidine-kinase (HK) receptor protein that binds to cytokinin, which is necessary for early procambial cell divisions in embryogenesis (Mähönen et al. 2000). Cytokinin response www.annualreviews.org • Plant Vascular Patterning 621 ARI 3 September 2010 20:17 occurs via a two-component signaling process in which the HK receptor transfers a phosphate to downstream response regulators (Hwang & Sheen 2001). Triple-knockout mutants for all three genes encoding CRE-family receptors, ahk2, ahk3, and wol/cre1/ahk4, as well as mutations in type-B response regulators ARR1, ARR10, and ARR12, exhibit similar vascular defects to those of wol mutants (Mähönen et al. 2000, Yokoyama et al. 2007). Furthermore, the vascular phenotypes of wol mutants are phenocopied by plants with depleted levels of cytokinins, such as transgenic lines expressing a CYTOKININ OXIDASE (CKX) under the control of a procambium-specific WOL/CRE1 promoter (Mähönen et al. 2000). Suppressor mutagenesis of wol mutants led to the identification of ahp6 mutants able to overcome the wol ability to form protoxylem (Mähönen Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. CB26CH24-Cano-Delgado et al. 2006a). ARABIDOPSIS HISTIDINE PHOSPHOTRANSFER PROTEIN 6 (AHP6) encodes a cytokinin signaling inhibitor that restricts the domain of cytokinin activity to permit protoxylem differentiation in a spatially specific manner. Collectively, these studies have demonstrated that cytokinin signaling has a key role in promoting and maintaining the identities of vascular cells other than protoxylem in the Arabidopsis primary root. TRANSCRIPTIONAL REGULATION OF VASCULAR CELL SPECIFICATION Recently, many transcriptional regulators responsible for vascular cell specification have been identified (Figure 5). Meristematic cells MP BDL ATHB-8 Vascular cells PHB, PHV, REV Micro RNA165/166 KAN1, KAN2, KAN3 Xylem Phloem XND1 APL ASL19/LBD30 ASL20/LBD18 EgMYB1 VND7 VND6 NST1, SND1/NST3 MYB20/42/43/52/54/58/63/69/85/103, SND2/3, KNAT7, EgMYB2 PXV MXV XF SE CC Figure 5 Transcriptional network during vascular cell specification. PXV, protoxylem vessel; MXV, metaxylem vessel; XF, xylary fiber; SE, sieve element; CC, companion cell. Arrows indicate activation; red inhibition lines indicate repression. 622 Caño-Delgado · · Lee Demura CB26CH24-Cano-Delgado ARI 3 September 2010 20:17 Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. HD-ZIP III/KAN/microRNA System Responsible for Early Vascular Development At the initiation of vascular development, an auxin-responsive transcriptional activator, MP, which belongs to a family of ARFs, regulates the specification of procambial cells through the direct activation of expression of ATHB-8, encoding one of the HD-ZIP III TFs (Donner et al. 2009). Although BODENLOS (BDL), an auxin-inducible transcriptional regulator, interacts with MP to suppress MP function in the absence of an auxin signal (Eshed et al. 2001), in the presence of auxin, BDL releases MP to activate the expression of downstream genes including ATHB-8, resulting in the initiation of vascular cell specification. In the shoot, xylem and phloem tissues are specified from the procambial cells through a fine regulation by two distinct classes of TFs: HD-ZIP IIIs and KANADIs (KANs), the latter of which are GARP-type TFs, which are closely associated with the determination of adaxial-abaxial polarity during plant development (Emery et al. 2003). In Arabidopsis, the simultaneous loss-of-function mutations in three HD-ZIP III genes, PHB, PHV, and REV, and in three KAN genes, KAN1 to KAN3, result in amphicribal (phloem surrounds xylem) and amphivasal (xylem surrounds phloem) vascular bundles, respectively (Emery et al. 2003), suggesting antagonistic functions for these HDZIP III and KAN genes in transcriptional regulation of xylem-phloem specification. It was also suggested that two other HD-ZIP III genes in Arabidopsis, ATHB-8 and ATHB-15/CORONA (CNA), function, at least in part, antagonistically to REV on the basis of an analysis of the rev athb-8 athb-15/cna triple mutant in which the defect in interfascicular fiber development in one of the rev mutant alleles (rev-6) was partially suppressed (Prigge et al. 2005). Because microRNA 165/166 specifically targets to the predicted sterol/lipid-binding START domains of HD-ZIP III mRNAs and then degrades the mRNAs, ectopic expression of microRNA 165/166 results in a significant reduction in the expression of these HD-ZIP III genes (Kim et al. 2005, Zhong & Ye 2007). Mutations in the microRNA-target sequences of HD-ZIP III genes without any alteration of the amino acid sequences, however, increases the stability of their transcripts that are accompanied by amphivasal vascular bundles (Emery et al. 2003, Juarez et al. 2004, McConnell et al. 2001, McHale & Koning 2004, Zhong & Ye 2004). Moreover, KAN genes might regulate HD-ZIP III expression negatively via microRNA 165/166 accumulation (Engstrom et al. 2004). In Zinnia cell cultures, the expression of the Zinnia homologs of Arabidopsis HD-ZIP III genes is enhanced during transdifferentiation of mesophyll cells into xylem TEs and is repressed by the application of BR biosynthesis inhibitors (Ohashi-Ito et al. 2002, Ohashi-Ito & Fukuda 2003). These data suggest that the HD-ZIP III/KAN/microRNA system orchestrates the transcriptional regulation of vascular tissue specification in response to auxin and BR signaling. Positive Regulators of Xylem Cell Specification Several TFs, including members of the LIM, MYB, and NAC families, have been identified as regulators of xylem cell development. NtLIM1, a member of the LIM TF family with a zinc-finger motif, specifically binds to the promoter sequence of lignin biosynthetic genes expressed in xylem and transiently activates transcription of the lignin biosynthetic genes in tobacco protoplasts (Kawaoka et al. 2000). Eucalyptus EgMYB2, a member of the R2R3-MYB TF family, binds to promoters of xylem-specific EgCCR and EgCAD2, which encode terminal enzymes of lignin biosynthesis; cinnamoylCoA reductase (CCR); and cinnamyl alcohol dehydrogenase (CAD); it also regulates the transcription of EgCCR and EgCAD2 (Goicoechea et al. 2005). The secondary cell walls of xylem fibers in tobacco plants overexpressing EgMYB2 are dramatically thickened with altered lignin profiles, suggesting that www.annualreviews.org • Plant Vascular Patterning 623 ARI 3 September 2010 20:17 EgMYB2 is a positive regulator of xylem cell development (Goicoechea et al. 2005). The NAC-domain TFs, VND1 to VND7, are expressed in the Arabidopsis in vitro xylem vessel inducible system in which subcultured suspension cells differentiate into xylem vessel elements at a high frequency in the presence of BL (Kubo et al. 2005). Of these, VND6 and VND7 have striking roles in regulating vessel cell specification in cooperation with other VND genes. The ectopic expression of VND6 and VND7 genes in Arabidopsis and poplar causes transdifferentiation of diverse cells such as epidermal cells, mesophyll cells, and guard cells into two different types of vessel cells similar to metaxylem vessels (VND6: with reticulate and pitted secondary cell walls) and protoxylem vessels (VND7: with annular and spiral secondary cell walls). Furthermore, a dominant repression of VND6 or VND7 by fusion with an artificial repressor domain (SRDX) inhibits vessel formation in the metaxylem or protoxylem of roots, respectively, and the expression of the C terminus–truncated VND7 protein under the control of the native VND7 promoter causes a strong inhibitory effect on the formation of all vessel types, as VND7 forms heterodimers with other VND proteins (Kubo et al. 2005, Yamaguchi et al. 2008). Two other Arabidopsis NAC-domain TFs, NAC SECONDARY WALL THICKENING PROMOTING FACTOR1 (NST1) and SECONDARY WALL ASSOCIATED NAC DOMAIN PROTEIN1 (SND1)/NST3, are expressed in xylary fibers and in interfascicular fibers that develop between the vascular bundles of inflorescence stems and act redundantly in the regulation of secondary cell wall thickening of these fibers (Ko et al. 2007; Mitsuda et al. 2005, 2007; Zhong et al. 2006, 2007b). Because VNDs, NST1, and SND1/NST3 phylogenetically belong to the same subfamily, it is plausible that these proteins have similar sets of downstream targets associated with the transcriptional network regulating secondary cell wall thickening. In fact, MYB46 and MYB83 are most homologous to EgMYB2, which has been proposed to regulate the expression of Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. CB26CH24-Cano-Delgado 624 Caño-Delgado · · Lee Demura lignin-related genes (Goicoechea et al. 2005), are common direct targets of these NACs, which redundantly function to turn on the entire secondary cell wall biosynthetic program in vessels and fibers (McCarthy et al. 2009; N. Nishikubo, Y. Nakano, and T. Demura, unpublished results). Moreover, several other TFs, including two NACs (SND2 and SND3), 10 MYBs (MYB20, 42, 43, 52, 54, 58, 63, 69, 85, and 103), and a Knotted-like homeobox protein (KNAT7), comprise the transcriptional network for secondary cell wall thickening (Zhong et al. 2007a, Zhong et al. 2007b, Zhou et al. 2009). Fine-Tuning of Gene Expression During Xylem Cell Specification Several other TFs play essential roles in finetuning gene expression programs that control xylem cell specification (Soyano et al. 2008). Two immature vessel-specific members of the Arabidopsis AS2/LDB family, AS2LIKE19 (ASL19)/LBD30 and ASL20/LBD18, function in a positive feedback loop system to maintain and promote the expression of VND7 required for vessel cell specification. Overexpression of ASL19/LBD30 and ASL20/LBD18 induces ectopic TE differentiation with ectopic expression of VND7. By contrast, expression of ASL20/LBD18 fused with the artificial repressor domain, SRDX, under the control of its native promoter results in formation of aberrant vessels, which suggests that these TFs regulate vessel cell specification positively. Furthermore, overexpression of VND6 and VND7 enhances the expression of ASL19/LBD30 and ASL20/LBD18, whereas dominant repression of VND6 and VND7 remarkably downregulates the expression of ASL19/LBD30 and ASL20/LBD18 (Soyano et al. 2008). XYLEM NAC DOMAIN1 (XND1), which is highly expressed in xylem (Zhao et al. 2005) and during in vitro vessel differentiation in Arabidopsis subcultured cells (Kubo et al. 2005), is a possible negative regulator of vessel cell specification (Zhao et al. 2008). Although XND1 knockout plants exhibit relatively normal Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. CB26CH24-Cano-Delgado ARI 3 September 2010 20:17 phenotype, overexpression of XND1 results in extreme dwarfism that is probably caused by the absence of vessel cells accompanied by little or no expression of two xylem-marker genes, XCP2 and XSP1 (Funk et al. 2002; Zhao et al. 2000, 2005). EgMYB1, a member of R2R3 MYB family preferentially expressed in the secondary xylem of Eucalyptus trees, binds specifically to ciselement MBSIIG, contained in the promoter of EgCCR, and represses the transcription of two lignin biosynthetic genes, EgCCR and EgCAD2 (Legay et al. 2007). These results suggest that EgMYB1 is a negative regulator of the lignin biosynthetic pathway during xylem cell development. Regulators of Phloem Cell Specification In contrast to our extensive knowledge of regulation of cell specification in xylem, there is a relative lack of information on regulation in phloem. APL, a member of the MYB family of TFs, is the only previously identified regulator of phloem cell specification (Bonke et al. 2003). APL is specifically expressed in immature phloem cells, and the apl mutant exhibits a seedling-lethal phenotype with a defect in phloem cell specification that results in the development of cells with characteristics of xylem vessel cells at the phloem poles, which are normally composed of two types of phloem cells, sieve elements and companion cells. Overexpression of APL in vascular cells prevents or delays xylem cell differentiation, suggesting that APL functions as a negative regulator of xylem cell specification in phloem positions, which might be mediated via a CLE/PXY pathway (see the section on Postembryonic Development of Vascular Tissues above). TOWARD COMPREHENSIVE REGULATORY NETWORKS AND SIGNALING IN VASCULAR TISSUE SPECIFICATION AND PATTERNING Genome-wide gene expression profiling data in vascular tissues in Arabidopsis, rice, Populus, and Zinnia have identified a plethora of genes that might be involved in the regulation of patterning and the specification of vascular tissues (Birnbaum et al. 2003, Brady et al. 2007, Demura et al. 2002, Jiao et al. 2009, Kubo et al. 2005, Schrader et al. 2004a). One of the next challenges is to unravel the underlying gene regulatory networks, which are also intercalated with complex hormone signaling processes during vascular tissue development. To address these questions, we need more visual and molecular tools in both current model species and more diverse plant species. Resolving complex gene regulation and signaling also requires more systematic inference of underlying mechanisms using mathematical models. Here we summarize recently developed tools and modeling approaches in plant vascular research. Cell Biology Resources: Vascular Cell Type–Specific Markers The inner localization of the vascular tissues and the lack of cell biology tools to trace vascular differentiation in intact plants have hampered the study of plant vascular development in the past. Initial genetic screenings based on overall root anatomy and histological staining of cell walls identified some key regulators of vascular patterning and differentiation (Bonke et al. 2003, Mähönen et al. 2000) and cell wall biosynthesis (Caño-Delgado et al. 2000, Turner & Somerville 1997). However, the lack of tools for easy visualization of plant vasculature has limited the identification of mutants with primary and/or specific defects in vascular development. The advent of GFPbased reporters has provided an important breakthrough in the study of vascular dynamics in intact plants (Figure 6). The identification and characterization of vascular cell type– specific markers allow for the study of vascular ontogeny in vivo (Scarpella et al. 2004, 2006; Wenzel et al. 2008) and serve as a basis for noninvasive screens of mutants with defects in vascular development (A.I. Caño-Delgado, unpublished results) and for the study of www.annualreviews.org • Plant Vascular Patterning 625 3 September 2010 b c d pSUC2-GFP pBRL1-YFPnls e f g h i pATHB-8-GUS pATHB-8-GUS J1721 pPP2-YFPnls pPXY-GUS j k l S4 S32 S29 m n o p q 100 μm Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. a 20:17 100 μm ARI 100 μm CB26CH24-Cano-Delgado r s t u A8 v pSULT2-YFPnls 626 Caño-Delgado · · Lee S18 Demura S20 Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. CB26CH24-Cano-Delgado ARI 3 September 2010 20:17 gene expression profiles using vascular cell type–based transcriptomics and proteomics (Birnbaum et al. 2003, Brady et al. 2007, Galbraith & Birnbaum 2006, Mustroph et al. 2009). The increasing number of vascular reporters available facilitates the genetic and molecular characterization of vascular patterning in Arabidopsis (summarized in Table 2). The initiation of leaf and root vascular primordia can be observed following procambium formation with the reporter expression of HD-ZIP III TF ATHB-8 (Baima et al. 1995; Scarpella et al. 2004, 2006). In the Arabidopsis root, ATHB8 traces the expression of provascular, quiescent center and columella cells, whereas it marks preprovascular patterning during leaf development (Figure 6). Similar reporters have been shown to trace the expression of procambial cells at both root and shoot inflorescence stems, such as ATHB-8’s closest homolog ATHB-15 (Ohashi-Ito & Fukuda 2003). The whole stele of the Arabidopsis primary root can be traced using the pWOL:GFP marker (Mähönen et al. 2000). Markers reflecting xylem differentiation such as pACL5:GUS and pXCP2:GUS specifically report xylem differentiation in several plant organs (Funk et al. 2002, Muñiz et al. 2008), whereas the expression of YFPnls or GUS driven by pVND7 and pVND6, respectively, in the root can efficiently trace the earlier stages of differentiation of both of protoxylem and metaxylem (VND7) and of centrally located metaxylem (VND6) during primary vascular development (Kubo et al. 2005; Figure 6). Markers S4, S18, S20, and S22 (Lee et al. 2006) tag root xylem vessels at different developmental stages (Figure 6). Phloem-associated tissues can be visualized in vivo by following the reporter expression of the proAPL:GUS/proAPL:GFP (Bonke et al. 2003, Mähönen et al. 2006a), pSUC2-GFP (Imlau et al. 1999), and pBRL1-GUS/pBRL1YFP markers (Caño-Delgado et al. 2004; A.I. Caño-Delgado, unpublished observations) (Figure 6) as well as root markers S29 and S32 (Lee et al. 2006). Interestingly, phloem markers such as pSUC2-GFP have proven to be valuable not only for the characterization of mutants with vascular anatomical defects but also for the identification of mutants with impaired intercellular transport functions in Arabidopsis (Benitez-Alfonso et al. 2009). ←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−− Figure 6 Expression of vascular reporters in different plant organs. pATHB-8:GUS expression (Baima et al. 1995) at the shoot apex of the leaf primordial of (a) 4-day-old and (b) 6-day-old plants. (c) pSUC2-green fluorescent protein (GFP) expression in the phloem cells of 6-day-old cotyledons (Imlau et al. 1999). The inset shows the vein patterning revealed by pSUC2-GFP expression in the phloem of the leaf of a 12-day-old plant. (d ) Detail of phloem expression in the vascular bundle of an inflorescence stem by a pBRL1-YFPnls marker (A.I. Caño-Delgado, unpublished research). (e) pATHB-8-GUS expression in the provascular cells, quiescent center (QC), and collumela cells at the primary root and ( f ) pATHB-8-GUS expression at the emergence of a lateral root primordia. ( g, h) Confocal median sections of J1751 marker expression at root provascular, QC, and collumela cells ( g); phloem marker pPP2-YFPnls expression in the differentiation zone of the root (h) (A. Caño-Delgado, unpublished observations). (i ) Detail of provascular expression in the vascular bundle of the inflorescence stem by pPXY-GUS marker (Fisher & Turner 2007). ( j, m) Longitudinal and radial confocal sections of AT3G25710 (S4)::GFP. GFP is specific to the xylem precursors. (k, n) Longitudinal and radial confocal sections of AT2G18380 (S32)::GFP. GFP is specific to the protophloem sieve cells. (l, o) Longitudinal and radial confocal sections of AT2G37590 (S32)::GFP. GFP is specific to the phloem precursors. ( p, q) pVND6-YFPnls ( p) and pVND7-YFPnls (q) expression in metaxylem and protoxylem (Kubo et al. 2005). (r) Longitudinal confocal sections of phloem marker pSULT2-YFPnls. (s) Longitudinal confocal sections of AT5G12870 (S18)::GFP. (t) AT1G71930 (S20)::GFP. GFP is specific to the differentiating xylem vessels. (u, v) AT3G48100 (A8)::GFP. GFP is specific to the procambium of the root meristem and the root cap (Lee et al. 2006). Propidium iodine (red ) was used as a counterstain. All root images were taken from 6-day-old plants. Pictures of pATHB-8-GUS and pPXY-GUS reporters are courtesy of G. Morelli and S. Turner. GFP, green fluorescent protein; GUS, β-glucuronidase; YFPnls, nuclear-localized yellow fluorescent protein. www.annualreviews.org • Plant Vascular Patterning 627 CB26CH24-Cano-Delgado ARI 3 September 2010 20:17 In addition to the promoter fusion markers, the study of the transactivation system using the GAL4-based enhancer trap has elicited numerous markers that exhibit vascular cell type–specific expression patterns at high temporal and spatial resolution (Bauby et al. 2007, Ckurshumova et al. 2009, Haseloff 1999, Haseloff et al. 1997). Theoretical Modeling for the Study of Vascular Patterning Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. Plant vascular patterning has attracted the attention of mathematicians for more than a century. Initially, the study of vascular patterning was merely theoretical and led researchers to propose several mechanisms for the regulation of vein formation in leaves (Meinhardt 1982, Mitchison 1981, Rolland-Lagan & Prusinkiewicz 2005), although experimental demonstrations of the plausibility of some of these mathematical simulations did not occur until recently (Benkova et al. 2003, Reinhardt et al. 2003). Sachs originally proposed the canalization hypothesis as a mechanism for differentiation of vascular strands connecting auxin sources to sinks (Sachs 1969). Based on this hypothesis, the formation of plant vascular networks is currently understood as an auxin-transport-based mechanism led by PIN1 protein accumulation and polarization (Sauer et al. 2006, Scarpella et al. 2006; for a recent review see Petrasek & Friml 2009). In recent years, mathematical predictions have also served to guide the genetic and cellular analysis of plant hormonal action in triggering organ initiation at the shoot, root, and vascular meristems (de Reuille et al. 2006, Grieneisen et al. 2007, Ibañes et al. 2009, Jonsson et al. 2006, Prusinkiewicz et al. 2009, Smith et al. 2006). By modeling auxin distribution, these studies demonstrated the relevance of PAT in creating the auxin maxima necessary for plant organogenesis. In relation to vascular patterning, work by Ibañes et al. (2009) has shown that periodic auxin maxima controlled by polar transport and not by the overall auxin level underlie vascular bundle spacing 628 Caño-Delgado · · Lee Demura (Figure 3). This innovative study provides evidence that PAT acts in connection with BR signaling. BRs have been proposed to modulate the procambial cell number needed to set the number of auxin maxima at the shoot vasculature (Ibañes et al. 2009). Another recent modeling example (Bayer et al. 2009) proposed a dual-polarization model for both phyllotaxis and the formation of leaf vascular strands and predicted transient apical polarization at the tip of the leaf midvein, which was confirmed by subsequent experiments in Arabidopsis and tomato plants. Interestingly, this model provides a unified view of phyllotaxis and vein initiation. Overall, these studies demonstrate the importance of mathematical analysis and computational modeling in advancing the understanding of diverse aspects of vascular development. Future studies should aim to develop a unified model that explains the initiation of vascular primordia at the shoot apex and its connection to various vascular organs in the plant. In years to come, the joint work between physicists and biologists will certainly disclose how the distinct factors controlling vascular morphogenesis integrate with other developmental processes, such as the formation of lateral shoot organs, lateral roots, and phyllotaxis, that contribute to overall plant architecture. Toolkits for the Understanding of Vascular Cell Specification and Differentiation In vitro cell and tissue culture systems could expand our knowledge of vascular cell development. Although no effective system has been developed to study phloem cell differentiation, several xylem cell differentiation systems offer us a chance to analyze the molecular mechanisms (Turner et al. 2007). The Zinnia system, in which mechanically isolated leaf mesophyll cells can be hormonally induced to transdifferentiate into TEs, has been studied from various perspectives, including hormonal control, cell-to-cell interaction, and global gene expression (Demura & Fukuda 2007, Fukuda 1997, Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. CB26CH24-Cano-Delgado ARI 3 September 2010 20:17 Fukuda & Komamine 1980, Turner et al. 2007). Although this system has proven to be valuable, the lack of an efficient transformation protocol limits its utility. Recently, a method to introduce DNA/RNA efficiently into Zinnia cells by electroporation-based transient transformation has been established (Endo et al. 2008). It was successfully used to identify two novel proteins, TED6 and TED7, which can modulate secondary cell wall formation of TEs, as potential components in the secondary cell wall synthesis machinery (Endo et al. 2009). Arabidopsis subcultured suspension cells can also be induced to form TEs in vitro in the presence of BL; global gene expression and microtubule dynamics have been described using this system (Kubo et al. 2005, Oda et al. 2005). The suspension cell cultures of tobacco and the callus cultures of radiata pine, both of which produce xylogenic cells with thickened secondary cell walls, also provide us with opportunities to analyze xylem cell differentiation in nonmodel systems (Millar et al. 2009, Wagner et al. 2007). Wood formation in tree species is an excellent model for understanding vascular development. Populus is accepted as a model tree species for several reasons, including the completion of genome sequencing (Tuskan et al. 2006), many molecular tools, including microarrays and genetic maps, the ease of genetic transformation, vegetative propagation, and genetic hybridization (Taylor 2002). Genome sequencing of Eucalyptus trees is also progressing (E. grandis in the United States and E. camaldulensis in Japan), which will allow us to expand our knowledge of wood formation. Expressed sequence tags generated from wood-forming tissues of other tree species increase our understanding of wood formation in combination with microarray-based gene expression analysis (Demura & Fukuda 2007). Because of difficulties in genetic transformation and the long lifetime of most tree species, it would be efficient to use transient gene introduction systems such as Agrobacterium-mediated introduction of transgenes into growing wood-producing tissue of Eucalyptus (Spokevicius et al. 2005). SUMMARY POINTS 1. Genetic screenings in Arabidopsis have identified several key regulators of vascular patterning. 2. Auxin distribution primes vascular initiation and maintains vascular vein continuity in the plant. 3. Brassinosteroids induce xylem differentiation in Zinnia cell cultures and contribute to vascular bundle patterning at the inflorescence stem of Arabidopsis. 4. Cytokinins control vascular cell proliferation as well as the differentiation of provascular cells into phloem and metaxylem. 5. A transcriptional network that controls vascular cell specification has been identified. 6. A systems biology approach that integrates novel molecular and cell biology tools, bioinformatics, and physics will further our understanding of vascular development and the evolution of vascular plants. FUTURE ISSUES 1. How are gene regulatory programs involved in vascular patterning related to those involved in the polarity of lateral organs? www.annualreviews.org • Plant Vascular Patterning 629 CB26CH24-Cano-Delgado ARI 3 September 2010 20:17 2. How does procambium/cambium contribute to the patterning and proliferation of vascular tissues? 3. What are the molecular mechanisms that drive the maturation of phloem, in particular cell elongation, enucleation, and communication between sieve cells and companion cells? 4. What is the hierarchy of hormonal action in the control of provascular cell specification, division, and differentiation? Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. 5. How are molecular mechanisms revealed in model systems conserved in nonmodel plants? DISCLOSURE STATEMENT The authors are not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review. ACKNOWLEDGMENTS This work was supported by the Boyce Thompson Institute and a National Science Foundation grant (IOS0818071) to J.Y.L., by a Grant-in-Aid for Scientific Research of Japan (Grant 21027031) to T.D., and by the Spanish Ministry of Science and Innovation (BIO2008/00505/) and the EU Marie Curie Initial Training Networks (ITN) FP7-PEOPLE-2007 to A.C.-D. LITERATURE CITED Aloni R. 1987. Differentiation of vascular tissues. Annu. Rev. Plant Physiol. 38:179–204 Asami T, Min YK, Nagata N, Yamagishi K, Takatsuto S, et al. 2000. Characterization of brassinazole, a triazole-type brassinosteroid biosynthesis inhibitor. Plant Physiol. 123:93–100 Baima S, Nobili F, Sessa G, Lucchetti S, Ruberti I, Morelli G. 1995. 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Plant Cell 21:248–66 www.annualreviews.org • Plant Vascular Patterning 637 AR425-FM ARI 14 September 2010 18:54 Contents Enzymes, Embryos, and Ancestors John Gerhart p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1 Annu. Rev. Cell Dev. Biol. 2010.26:605-637. Downloaded from www.annualreviews.org by Universitat Autonoma de Barcelona on 12/09/13. For personal use only. Control of Mitotic Spindle Length Gohta Goshima and Jonathan M. Scholey p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p21 Annual Review of Cell and Developmental Biology Volume 26, 2010 Trafficking to the Ciliary Membrane: How to Get Across the Periciliary Diffusion Barrier? Maxence V. Nachury, E. Scott Seeley, and Hua Jin p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p59 Transmembrane Signaling Proteoglycans John R. 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