Plant Mol Biol (2009) 69:347–360 DOI 10.1007/s11103-008-9374-9
Hormone interactions during vascular development Jan Dettmer Æ Annakaisa Elo Æ Yka¨ Helariutta
Received: 2 April 2008 / Accepted: 1 July 2008 / Published online: 25 July 2008 Ó Springer Science+Business Media B.V. 2008
Abstract Vascular tissue in plants is unique due to its diverse and dynamic cellular patterns. Signals controlling vascular development have only recently started to emerge through biochemical, genetic, and genomic approaches in several organisms, such as Arabidopsis, Populus, and Zinnia. These signals include hormones (auxin, brassinosteroids, and cytokinins, in particular), other small regulatory molecules, their transporters, receptors, and various transcriptional regulators. In recent years it has become apparent that plant growth regulators rarely act alone, but rather their signaling pathways are interlocked in complex networks; for example, polar auxin transport (PAT) regulates vascular development during various stages and an emerging theme is its modulation by other growth regulators, depending on the developmental context. Also, several synergistic or antagonistic interactions between various growth regulators have been described. Furthermore, shoot–root interactions appear to be important for this signal integration. Keywords Vascular meristem HD-ZIPIII genes Auxin Cytokinin
Jan Dettmer and Annakaisa Elo contributed equally. J. Dettmer A. Elo Y. Helariutta (&) Plant Molecular Biology Laboratory, Department of Biological and Environmental Sciences, Institute of Biotechnology, University of Helsinki, P.O. Box 56, 00014 Helsinki, Finland e-mail:
[email protected] Y. Helariutta Department of Forest Genetics and Plant Physiology, Umea˚ Plant Science Center, Swedish University of Agricultural Sciences, 90183 Umea, Sweden
Introduction The vascular tissues serve two main functions; they give physical structure and support to plants, and deliver water and nutrients as well as other substances needed for growth and defense. Vascular tissues form bundles, which interconnect all parts of the plant, extending from the stem into leaves, and down into the root system. They typically have two fully differentiated, conductive tissue types, xylem and phloem, as well as some undifferentiated procambial cells with pluripotent characteristics. Xylem transports water and dissolved minerals, whereas phloem is required for the distribution of mainly photosynthetic products (sugars, RNA, proteins, and other organic compounds) from source to sink organs. Vascular development begins when a specific set of asymmetric cell divisions establish the innermost domain of the embryonic root/hypotocyl and cotyledons as preprocambial tissues in vascular bundles. The same process is recapitulated when lateral organs are established post embryogenesis (Fig. 1a). Later during embryogenesis the preprocambial tissue is patterned, defining domains for xylem, phloem, and the intervening pluripotent procambium in an organ-specific manner (Fig. 1b). Further development in the xylem and phloem domains leads to the differentiation of conductive tissues (Fig. 1c). After germination this so-called primary vascular pattern is propagated by the root and shoot apical meristems (Fig. 1c, d). Later in the plant life cycle, some of the intervening pluripotent procambial cell files, as well as the interfascicular cell files in shoot and pericycle cell files in the root undergo further periclinal asymmetric cell divisions and establish the lateral meristem, vascular cambium that is characteristic of the secondary phase of plant development (Fig. 1d). This meristem produces secondary xylem and
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Fig. 1 Organization of the vascular tissues during the primary and secondary developmental phases in higher plant, schematic view. (a) Cross section of early developing leaf. Preprocambial cells precede the vascular development. (b) Cross section of leaf. Within the vascular strands primary xylem and phloem tissues differentiate asymmetrically from the procambium. (c) Primary development shown in stem cross section. (d) Organization of vascular tissues during the secondary phase of vascular development. During this phase cambial cells proliferate and secondary xylem and phloem are formed. (e) Cross section of root tip showing vascular organization during primary development. Later during development root vascular tissues proceed also into the secondary development phase (not shown in figure)
phloem and increases the girth of the plant organs. A characteristic feature of the vascular bundles is the presence of an undifferentiated pluripotent tissue. Our understanding of this tissue (whether it be preprocambium, procambium or vascular cambium) in various developmental contexts is limited, and therefore at this stage it may be appropriate to talk about ‘‘vascular meristem’’, which covers collectively the various developmental phases of this pluripotent tissue. Knowledge about the developmental control of vascular patterning is still relatively poor compared with that of the other plant tissues. Molecular and genetic studies with Arabidopsis thaliana mutants and
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cellular studies with Zinnia elegans xylogenic cultures and molecular studies of the vascular cambium in poplar trees have started to reveal several of the signals and their interactions at the molecular level. Various molecular components controlling vascular development have been recently reviewed by several authors (Ye 2002; Mattsson et al. 2003; Fukuda 2004; Scarpella and Meijer 2004; Carlsbecker and Helariutta 2005; Samuels et al. 2006; Sieburth and Deyholos 2006; Turner et al. 2007). In this review we will focus on the emerging knowledge on how these components might interact to specify a regulatory network underlying vascular development.
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Vascular bundle formation A number of studies have shown that polar auxin transport is required for continuous vascular pattern formation and establishment of procambial strands (Mattsson et al. 2003; Scarpella et al. 2006; Berleth et al. 2007). Sachs (1981) proposed the auxin-flow canalization hypothesis, which suggests that the amplification of auxin transport capacities by positive feedback loop in some cells leads to establishment of a directional intercellular transport mechanism. This, in turn, promotes auxin transport, leading to the canalization of auxin flow along a narrow column of cells. This continuous polar transport of auxin through cells ultimately results in the differentiation of strands of procambial cells and, subsequently, vascular strands (Fig. 2a). The major auxin efflux related protein, PIN-FORMED1 (AtPIN1), is expressed in meristematic ground cells prior to appearance of vascular tissue specific markers in domains that become restricted towards sites of vascular bundle formation (Scarpella et al. 2006). During vein formation in leaves, the progenitor cells (‘‘pre-procambial’’ cells) are formed from subepidermal leaf ground cells. Following the determination of vascular identity, the vascular strands are patterned and the newly formed vascular cells divide and elongate along a common axis, which is essential for the formation of a continuous vein network that can carry out its various transport roles (Scheres and Xu 2006). At the apex of leaf primordia, subcellular AtPIN1 polarity indicates that auxin is directed along the epidermis to distinct ‘‘convergence points’’ and its subsequent expression in subepidermal cells precedes the formation of vascular strands (Scarpella et al. 2006). Experiments suggest that this convergence point positioning is a self-organizing auxin transport-dependent process (Scarpella et al. 2006). Transcription of auxin-inducible genes is mediated by members of the auxin response factor (ARF) family. In the absence of auxin, the transcription of auxin-inducible genes is blocked by the dimerization of Aux/indole-3-acetic acid (IAA) proteins with ARFs. In the presence of auxin Aux/IAA proteins are degraded via the ubiquitin-proteasome pathway. Auxin binds to TIR1, an F-box protein (and its close relatives), which recruits the Aux/IAA to the ubiquitin protein ligase SKP1/CULLIN/ F-box (SCF) complex. Following ubiquitination and final degradation of Aux/IAA allows ARFs to form homodimers and promote transcription (Kepinski and Leyser 2005; Dharmasiri et al. 2005; Wenzel et al. 2007). Genetic screens for vein-pattern-defective mutants have identified several genes that regulate auxin transport or signal transduction. Mutations in the auxin response genes MONOPTEROS (MP)/AUXIN RESPONSE FACTOR 5 (ARF5), AUXIN RESISTANT 6 (AXR6), and BODENLOS(BDL)/IAA12 cause a discontinuous venation pattern associated with improper
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vascular differentiation (reviewed in Mattsson et al. 2003). Expression of MP and PIN1 precede vascular formation, suggesting that both proteins are important components in auxin canalization and thus leaf vein formation (Wenzel et al. 2007; Hardtke and Berleth 1998). The van3 mutation causes the so-called vascular island phenotype, in which the connection of the vascular network is disrupted. Scarpella et al. (2006) reported that the onset of fragmentation in van3 mutant is reflected already in a gradual decay of the PIN1 expression, suggesting that the corresponding gene has a role in the maintenance of PAT and promoting vascular continuity through PIN genes. VAN3 encodes an auxinresponsive adenosine diphosphate (ADP)-ribosylation factor–guanosine triphosphatase (GTPase)-activating protein (ARF–GAP) (Koizumi et al. 2005). In asymmetric leaf 1 and 2 mutants the venation pattern is reduced throughout the leaf blades compared with wild type. This correlates with the asymmetric localization of auxin signaling at the distal leaf tip, marked by changes in DR5::GUS expression, suggesting that symmetrical auxin distribution within the developing leaf controls both vascular pattern and the pattern of cell divisions (Zgurski et al. 2005). In addition to auxin, sterols have been shown to be involved in the formation of vascular patterning in leaves (Fig. 2a, Scarpella and Meijer 2004). An Arabidopsis mutant called cotyledon vascular pattern1 (cvp1) has a phenotype where a discontinuous, poorly axialized venation pattern is formed. The gene corresponding to this mutation was reported to be STM2, a sterol methyltransferase and it is important to balance the levels of sterol and brassinosteroid (Carland et al. 2002). A link between sterols and auxin polarity maintenance has been documented based on the sterol methyltransferase 1 (stm1/orc) mutants. The orc mutant was identified due to defects in root patterning, but also showed an abnormal venation pattern with discontinuous vascular strands, similar to those in other mutants reported to display defects in vascular patterning (Scheres et al. 1996). It was shown that in this mutant AtPIN1 and AtPIN3 proteins were mislocalized, whereas the polar positioning of the influx carrier AUX1 appeared normal, suggesting that balanced sterol composition is required for cell polarity, auxin efflux, and vascular patterning in Arabidopsis (Willemsen et al. 2003). This finding was later supported by Men et al. (2008), who showed that correct membrane sterol composition is essential for the acquisition of PIN2 polarity. Genetic screens for Arabidopsis mutants with defects in vein patterning, including reduced vein number or free vein endings, have revealed signaling molecules other than hormones. Several of these are likely to interact with hormones either through cell–cell communication or by affecting the production of, transport of, or response to hormonal signals (Scarpella and Meijer 2004; Sieburth and
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Fig. 2 Hormone interaction during different phases of vascular tissue development. (a) The earliest event of vascular bundle formation is establishment of the procambium. Polar auxin transport (PAT), which is established by the polar localization of PIN proteins, is required to determine the zone of procambium formation. Both auxin and sterols modulate PAT and influence the earliest step of vascular tissue formation. Cytokinins modulate PAT during lateral root development. Whether the same happens during vascular development is not known. (b) The two conducting vascular tissues phloem and xylem are arranged in an organ-specific pattern. In the vascular bundles of the shoot, HD-ZIPIII genes and KANADI genes determine the abaxial and the adaxial position of phloem or xylem, respectively. In phb phv rev triple mutants phloem surrounds xylem and in gain-of-function HD-ZIPIII mutants and kan1 kan2 kan3 triple mutants xylem surrounds phloem. Thus, HD-ZIPIII and KANADI genes antagonize each other. Further regulation of the HD-ZIPIII genes occurs via miR165/166, auxin, and brassinosteroids (BR). AtHB8 expression is stimulated by auxin. In embryos proper expression of both gene families is required to establish auxin maxima via PAT at the right
position. Whether this happens also more specifically in the vascular tissues is not known. Furthermore, HD-ZIPIII genes promote expression of the BR receptor BRL3. (c) The vascular meristem gives rise to phloem and xylem cells. Auxin and cytokinins have been implicated in both specification and activity of the cambium. Also gibberellins (GA) are positive regulators of cambial activity. GA appears to promote PAT, as GA induces PIN1 expression in cambium of poplar. Furthermore, auxin stimulates GA biosynthesis genes and inhibits GA degradation genes. An as yet unknown flowering-related signal from the shoot promotes the late stage of cambial activity. (d) The last phase in vascular tissue development is differentiation of the conductive tissues. To obtain the ring-like secondary wall pattern of the xylem at protoxylem position, cytokinin signaling has to be inhibited by AHP6. Xylogen controls xylem differentiation and is positively regulated by both auxin and cytokinin. VND6 and VND7 determine differentiation into meta- and protoxylem, respectively. Both transcription factors are positively regulated by auxin, cytokinin, and brassinosteroids. See text for references
Deyholos 2006). Cotyledon vascular pattern 2 (cvp2) mutants exhibit an increased number of free vein endings and resulting is an open-vein network. The gene CVP2, which seems to have a critical role in the propagation of procambial strand formation, encodes an inositol polyphosphate 59 phosphatase (5PTase). This molecule has
been shown to regulate inositol signaling and acts as a second messenger (Carland and Nelson 2004). The polaris (pls) mutants have a short-root phenotype and reduced vascularization of leaves; pls roots are hyperresponsive to exogenous cytokinins and show increased expression of the cytokinin-induced gene ARR5/IBC6 compared with wild
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type (Casson et al. 2002). PLS produces a short (500nucleotide) auxin-inducible transcript and encodes a predicted polypeptide of 36 amino acid residues which may function through cytokinin and auxin homeostasis (Casson et al. 2002). BYPASS1 (BPS1), an Arabidopsis gene of unknown function, is required to prevent constitutive production of a root-derived signal that inhibits leaf initiation, leaf expansion, and shoot apical meristem activity and a recessive mutation in this gene results in, e.g., defects in leaf vein patterning (Van Norman et al. 2004). This longdistance signal, which apparently is an as yet unidentified carotenoid-derived molecule, might influence vein patterning by inhibiting auxin responses, since bps1 leaves do not show auxin-inducible DR5::GUS expression (Van Norman et al. 2004; Sieburth and Deyholos 2006).
Patterning of vascular bundles The different cell types within the vascular system are arranged in an organ-specific pattern (Fig. 1). In the stem and leaves of Arabidopsis, xylem forms at the internal/ upper (adaxial) pole, whereas phloem develops on the peripheral/lower (abaxial) pole of the vascular bundles. Adaxial–abaxial polarity of lateral organs and vascular tissue of the shoot is established by two gene families antagonizing each other, the plant-specific class III homeodomain-leucine-zipper-containing (HD-ZIPIII) transcription factors [PHABULOSA (PHB), REVOLUTA (REV), PHAVOLUTA (PHV), CORONA (AtHB15) and AtHB8] and the KANADI [KAN1-3] GARP transcriptional regulators. The idea of an antagonistic interaction is based on the observation that gain-of-function mutants of HDZIPIII members (rev-10D, phb-d, phv-d) and triple kan1 kan2 kan3 loss-of-function mutants have adaxialized lateral organs and vascular bundles in which xylem surrounds phloem. Furthermore, the opposite phenotype within vascular bundles, in which phloem surrounds xylem, is found in triple rev phb phv loss-of-function mutants (Fig. 2b) (Eshed et al. 2001; Kerstetter et al. 2001; McConnell et al. 2001; Emery et al. 2003; Juarez et al. 2004; McHale and Koning 2004; Zhong and Ye 2004). All gain-of-function HD-ZIPIII mutations map to a miRNA165/166 target sequence within a putative sterol/lipid-binding StART [StAR (steroidogenic acute regulatory protein)-related lipid transfer] domain (Mallory et al. 2004; McConnell et al. 2001; Emery et al. 2003; Juarez et al. 2004; McHale and Koning 2004; Zhong and Ye 2004). It was speculated that KANADI would mediate the negative regulation of HDZIPIII expression by regulating miRNA165/166 (Bowman 2004). However, no such observation has been published yet, suggesting that it is equally possible that miRNA and KANADI might regulate class III HD-ZIP gene expression
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independent from each other. Recently a post-transcriptional regulatory mechanism via a new gene family called LITTLE ZIPPER (ZPR) was identified. By forming heterodimers with REV the ZPR proteins prevent it from binding to DNA (Wenkel et al. 2007). Thus, the LITTLE ZIPPERs provides an alternative mode of regulation. Also hormones have been implicated to interact with members of both gene families (Fig. 2b). It was shown that auxin can induce the transcription of at least one of the HDZIPIII genes (AtHB8) (Baima et al. 1995; Mattson et al. 2003), whereas PHV, PHB, and REV do not appear to be regulated by auxin (Mattson et al. 2003). Further evidence that AtHB8 expression is regulated by auxin comes from the observation that during leaf vein patterning PIN1 expression precedes procambium formation and AtHB8 expression (Scarpella et al. 2006). The auxin response factors ETT (ETTIN, ARF3) and ARF4 seem to promote abaxial identity together with KANADI or its downstream targets (Pekker et al. 2005). Also lateral root formation, which is initiated by auxin is altered in KANADI loss of function and REV gain of function mutants (Hawker and Bowman 2004). Recently it was shown by Izhaki and Bowman that polar auxin transport (PAT) is affected in embryos of multiple loss-of-function mutants of both gene families (Fig. 2b) (Izhaki and Bowman 2007). Polar localization of PIN proteins during embryogenesis is required to direct auxin flow (and form auxin maxima) to establish the apical-basal axis and bilateral symmetry (Friml et al. 2003; Weijers et al. 2005). In kan1 kan2 kan4 embryos, changes in the expression pattern and polar localization of PIN1 can be observed. This results in the formation of ectopic areas of auxin accumulation, which coincided with the sites of leaflike hypocotyls outgrowths. In phb phv rev heart-stage embryos, the bilateral expression pattern of PIN normally observed in wild type was lacking. Instead, the altered PIN1 expression pattern suggests that the auxin flow is channeled towards a central apical point, resulting in the formation of one auxin maximum, which leads to the formation of only one cotyledon primordium. To further explore the antagonistic roles of HD-ZIPIIIs and KANADIs during embryo development a hexatuple kan1 kan2 kan4 phb phv rev mutant was generated. Interestingly, whereas phb phv rev mutants lack a bilateral pattern (formation of only one cotyledon), the kan1 kan2 kan4 phb phv rev seedlings have two cotyledons with abaxial outgrowths and ectopic leaf-like outgrowths forming from the hypocotyls similar to those in the kan1 kan2 kan4 mutant. Thus, loss of KANADI activity in the phb phv rev background mitigates the loss of bilateral symmetry. However, the hexatuple mutant also forms a single radial leaf-like organ at the position of the shoot apical meristem (SAM). The proximal vascular bundles in this central leaf-like organ is
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radialized, with phloem surrounding xylem in the center (Izhaki and Bowman 2007). This vascular arrangement can be seen in radial phb phv rev cotyledons (Emery et al. 2003). It remains to be defined how these interactions between HD-ZIPIIIs, KANADIs, and auxin-controlling organ polarity relate to patterning of vascular bundle. Besides miRNA165/166 and auxin, brassinosteroids (BR) have been implicated in positively regulating the expression of HD-ZIPIII genes (Fig. 2b). The Zinnia elegans mesophyll cell culture offers a valuable tool to investigate xylogenesis. With this system mesophyll cells can be triggered with auxin and cytokinins to transdifferentiate into xylem vessels (Fukuda and Komamine 1980). Using this cell culture system, it was shown that brassinosteroid levels increase prior to differentiation into xylem tracheary elements (Yamamoto et al. 2001). As the cell culture is initiated to differentiate into xylem cells, transcripts of HD-ZIPIII genes accumulate. Pharmacological inhibition of brassinosteroid biosynthesis in these cells blocks HD-ZIPIII expression. Addition of BR restored the transcript level (Ohashi-Ito et al. 2002). In Arabidopsis overexpression of the Zinnia homologues of AtHB8 and REV containing a mutation in the StART domain resulted in an increased number of xylem cells (Ohashi-Ito et al. 2005). Taken together, this indicates that brassinosteroids promote xylem formation by enhancing HD-ZIPIII genes expression (Fig. 2b). Furthermore overexpression of one Zinnia HD-ZIPIII gene resulted in upregulation of the brassinosteroid receptor BRI1-like 3 (BRL3) and a BAK-like leucine-rich repeat receptor-like kinase (LRR-RLK), indicating that HDZIPIII genes promote brassinosteroid signaling (Fig. 2b) (Ohashi-Ito et al. 2005). That brassinosteroids (BR) have an important role in vascular tissue formation in Arabidopsis has been shown in BR-deficient mutants (cpd; dwf7) (Szekeres et al. 1996; Choe et al. 1999) and perception mutants (Cano-Delgado et al. 2004). By searching for sequence similarities with the BR receptor BRI1 (BRASSINOSTEROID INSENSITIVE 1) a leucine-rich repeat receptor kinase (Wang et al. 2001; Kinoshita et al. 2005), three BRI1-like (BRL) genes were identified. However, when expressed under the control of the BRI1 promoter, only BRL1 and BRL3 but not BRL2 could complement the weak bri1-301 mutant. Using a BR-binding assays Cano-Delgado A. et al. showed that BRL1 and BRL3 bind brassinosteroid with high affinity. Interestingly, both BRL1 and BRL3 are expressed in the vasculature of all organs, with BRL3 specifically expressed in the phloem. Analysis of the three BR receptor mutants suggests that these function redundantly to control differentiation of the vasculature (Cano-Delgado et al. 2004).
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Fig. 3 Interaction between cytokinin signaling and its inhibitor AHP6. (a) Schematic view of Arabidopsis root vasculature. Left: transverse section of WT primary root; middle: wol root with reduced amount of all-protoxylem identity cells in stele; and right: ahp6 root showing unstable protoxylem specification. (b) A model showing the reciprocal interaction of cytokinin signaling and AHP6 that regulates the cell fate decision between the maintenance of procambial cell identity (PC) and the differentiation of protoxylem elements (PX) (according to Ma¨ho¨nen et al. 2006a)
Specification and maintenance of vascular meristem Several factors with distinct roles during various aspects of vascular meristem activity have been identified. Cytokinin signaling appears to regulate both the specification of pluripotent cell identity as well as cell proliferation during (pro)cambial activity (Fig. 2c). The recessive wol mutation results in reduced cell proliferation and exclusive differentiation of the cell files within the pericycle layer as protoxylem (Fig. 3a; Scheres et al. 1995; Ma¨ho¨nen et al. 2006a). Molecular analysis revealed that the wol mutation maps to the CRE1 gene, which encodes the cytokinin receptor CRE1/WOL/AHK4 (Inoue et al. 2001; Ma¨ho¨nen et al 2000). This receptor was shown to bind cytokinin species and this binding was abolished in the wol mutant (Yamada et al. 2001). CRE1/WOL is a member of a small gene family consisting two additional members, AHK2 and AHK3, which share expression within the vasculature (reviewed, e.g., by Bishopp et al. 2006). The three histidine kinases act as receptors by activating a phosphorylation cascade characteristic of prokaryotic two-component signaling. In this signal transduction the phosphorylation signal is first transferred to the nucleus by the histidinephosphotransfer proteins (AHP1-5), which activate specific transcription factors, the type-B ARABIDOPSIS RESPONSE REGULATORS (ARRs) (reviewed by Mu¨ller and Sheen 2007). It has been shown that among the seven type-B ARR members ARR1, ARR10 and ARR12 play the general role in cytokinin signaling, since loss of functional alleles of all of these three genes results in wol-like phenotype (Ishida et al. 2008). Type-B ARRs receive the phosphoryl group from AHPs activating the transcription
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of cytokinin primary response genes, including type A ARRs (Hwang and Sheen 2001). Several of the type A ARRs have been found to act as negative regulators in a cytokinin signaling feedback loop (Kiba et al. 2003). Rashotte et al. (2006) demonstrated that in response to cytokinin also a subgroup of AP2 transcription factors designated as cytokinin response factors (CRFs) move into the nucleus, and that they mediate, together with the type B ARRs, the transcriptional response to cytokinin. CRE1/WOL/AHK4 is expressed specifically in the vascular cylinder of the root from early embryogenesis, which supports the idea of cytokinin signaling regulating cell specification and/or cell proliferation during vascular development. Either the triple cre1 ahk2 ahk3 loss-offunction mutant, or transgenic lines ectopically expressing a cytokinin degrading enzyme, cytokinin oxidase, results in phenocopy of wol (Ma¨ho¨nen et al. 2006a, b; Higuchi et al. 2004). This indicates that cytokinin signaling is required to promote and maintain cell identities other than protoxylem, and in the absence of cytokinin signaling, protoxylem is the default identity (Ma¨ho¨nen et al. 2006a). This view was further consolidated by the analysis of an extragenic second-site suppressor mutations of wol at the AHP6 locus, leading to a partial suppression of the all-protoxylem wol phenotype (Ma¨ho¨nen et al. 2006a). The ahp6 mutants display a distinct phenotype in the root vascular bundle, in which protoxylem differentiation occurred sporadically along the root (Fig. 3a). The AHP6 locus encodes for an AHP family protein lacking the conserved histidine residue critical for phosphorelay and is thus called a ‘‘pseudo’’ phosphotransfer protein (Ma¨ho¨nen et al. 2006a). Consequently, AHP6 acts as an inhibitor to cytokinin signaling and regulates the balance of cell proliferation and differentiation early during vascular development (Fig. 3b). AHP6 is expressed in protoxylem and the adjacent pericycle cell lineages and AHP6 expression is detectable early during embryogenesis in the early torpedo stage of both wild-type and wol embryos (Ma¨ho¨nen et al. 2006a). The mutant phenotypes as well as expression pattern support the idea that cytokinin signaling specifies the spatial domain of AHP6 expression upstream of protoxylem differentiation, and therefore cytokinin is required for the proper vascular development already during the early phases of embryogenesis. It was recently shown that CRE1/WOL is a bifunctional kinase/phosphatase, whose activity on the phosphoload of the signal transduction depends on the status of cytokinin binding (Ma¨ho¨nen et al. 2006b). Under high cytokinin concentration the prevailing kinase activity by CRE1/WOL results in phosphorylation of the phosphotransfer intermediate substrates, which relay the phosphate further to the nuclear response regulators. Under low cytokinin concentration the prevailing activity by CRE1/WOL is
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dephosphorylation. Since the wol mutation dramatically impairs the binding of cytokinin ligands and since CRE1/ WOL is the most active member of the gene family during root development (based on gene expression level), wol results in constitutive phosphatase activity of the receptor regardless of ligand binding, and thus exclusive protoxylem differentiation. AHK2 and AHK3 do not appear to have the phosphatase activity. When CRE1/WOL was replaced by AHK2 under the pCRE1 promoter, higher cytokinin responsiveness was achieved (Ma¨ho¨nen et al. 2006b). Secondary development and vascular cambium is initiated earlier in these plant lines than in wild type, indicating that in addition to cell specification, cytokinins also have a role in regulating the rate of cell proliferation associated with cambial activity. Cytokinin signaling may also control cell proliferation by activating various regulatory pathways. One candidate as a target of cytokinin signaling is LONESOME HIGHWAY (LHW). Mutations in this gene eliminate bilateral root symmetry and reduce the number of cells in the center of the root, resulting in roots with only single xylem and phloem poles. Like cytokinin, LHW is required to promote cell proliferation in the stele; however, LHW is also required to promote protoxylem formation (Ohashi-Ito and Bergmann 2007). It remains to be seen how the LHW and cytokinin signaling relate to each other in regulating cell proliferation and specification during procambium development. The maintenance of the pluripotent identity of stem cell is crucial for meristem function. In the Arabidopsis shoot meristem, the stem cell population is regulated by a dynamic feedback mechanism between WUSCHEL (WUS) and CLV genes. The function of the homeobox box transcription factor WUS, is to maintain stem cell identity and mutations in WUS result in the misspecification of stem cells and termination of shoot and floral meristems after a few organs have been formed (Laux et al. 1996). In contrast, recessive mutations in the three CLV genes, CLAVATA1, 2, and 3 result in delayed organ initiation, leading to an accumulation of meristem cells and to a gradual increase in size of the shoot meristem dome (Clark et al. 1993, 1995). The three CLV genes encode components of a receptor kinase signaling pathway, in which CLV1 represents a putative receptor kinase, CLV2 a leucine-rich repeat accessory protein component, and CLV3 a putative signaling peptide. Thus, it can be concluded that the CLV receptor-ligand complex promotes cell differentiation form the meristem (Clark et al. 1993, 1995; Kayes and Clark 1998). WUS has been identified as a key target of the CLV meristem signal transduction feedback loop where the activity of the plasma-membrane-bound CLV complex leads to the downregulation of WUS transcription which restricts the size of the WUS expression domain in the
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organizing center (Schoof et al. 2000). Recently, it was shown that stem cell maintenance in the root apical meristem is regulated by a WUS homologue, WOX5, indicating that stem cell maintenance signaling in both shoot and root apical meristems employs related regulators (Sarkar et al. 2007). Could the CLV-WUS-like regulon also operate in maintaining the vascular meristem? The experimental evidence obtained so far supports this theory. The activity of SAM maintenance genes has not been confirmed in vascular meristems in expression profiling studies (Ko and Han 2004; Schrader et al. 2003). Instead expression of the two WUS-related genes PttHB2 and PttHB3 was found in poplar cambium array study (Schrader et al. 2003) and recently a CLV1-like receptor kinase was reported to be required to maintain normal polar cell divisions of the procambium and spatial organization of vascular development in Arabidopsis. Plants carrying mutation in this locus showed poor spatial separation of xylem and phloem and were thus named pxy (phloem intercalated with xylem) (Fisher and Turner 2007). Also, members of the CLE (CLAVATA3(CLV3)/ENDOSPERM SURROUNDING REGION (ESR)) peptide family involved in vascular development have been characterized. The CLE peptide family includes the putative CLV1 ligand, CLV3, which is the suppressor of stem cell proliferation in the SAM (reviewed in Fukuda et al. 2007). CLE41/44 and CLE42 have been documented to promote maintenance and/or proliferation of procambial cells and to repress differentiation from procambial cells to tracheary elements (Ito et al. 2006). It is possible that CLE42 and/or CLE44 act as ligands for PXY or still unidentified CLV1-like receptorlike kinase in cambium, maintaining the stem cell population in cambium. During the past 10 years, interactions between several of SAM maintaining factors and various hormones have been identified. Several type A response regulators (ARRs), which act in a negative feedback loop of cytokinin signaling, have been shown to be negatively regulated by WUS and positively regulated by its feedback regulator, CLV3 (Leibfried et al. 2005). WUS directly represses the transcription of several two-component ARABIDOPSIS RESPONSE REGULATOR genes (ARR5, ARR6, ARR7, and ARR15), which act in the negative feedback loop of cytokinin signaling. It remains to be studied whether analogous interactions occur during vascular development. As described above, auxin and PAT regulate several successive processes of vascular development. Auxin also has a well-established role in maintaining the vascular cambium (Fig. 2c). Pharmacological experiments performed using sunflowers in the 1930s and 1940s showed that an exogenous source of IAA could replace the apical shoot in inducing cell divisions in the cambium and differentiation of the secondary xylem (Snow 1935;
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Gouwentak 1941). More recent data confirmed these early observations in different model plants and established that the shoot apex is the major source of auxin in the cambial zone (Tuominen et al. 1997; Uggla et al. 1998). Furthermore, it was shown that during wood development an auxin gradient is formed which has its maximum in the cambial zone (Uggla et al. 1996; Tuominen et al. 1997). The localization of two PIN proteins (PttPIN1 and PttPIN2) in the cambium of poplar stems further suggests that the cambium is the major site of PAT (Schrader et al. 2003). This radially oriented gradient of basipetal auxin transport has since been shown to also accompany specific expression patterns of auxin-signaling-related genes in the region (Moyle et al. 2002). During transition to cambial dormancy, polar auxin transport is reduced and cambium is rendered insensitive to exogenously applied auxin (Schrader et al. 2003). Additionally, auxin has been indicated to mediate a signal perceived in cambium relating to plant body mass. Weight of stem seems to have a prominent positive effect on the cambial activity, as has been shown by Ko et al. in Arabidopsis inflorescence stems. In that study it was reported that weight stimulus facilitates auxin transport and subsequently promotes development of secondary xylem (Ko and Han 2004). Further evidence for the function of auxin as a positive regulator of cambial activity is provided by INTERFASCICULAR FIBERLESS/ REVOLUTA ifl Arabidopsis mutants. In these mutants, downregulation of auxin transporter expression resulted in dramatically reduced basipetal auxin flow and consequently reduced cambial activity at the basal parts of inflorescence stems (Zhong and Ye 2001). As auxin and cytokinins appear to be the key phytohormones specifying several aspect of vascular development tight crosstalk between these hormones is needed. The exact mechanisms of these interactions have been, however, unclear. Recently an interaction mode between auxin and cytokinin has been revealed in the context of root meristem organization and lateral root initiation in Arabidopsis. It was found that cytokinins act on auxin homeostasis by changing auxin transport (in the case of lateral root development via the downregulation of PIN gene expression) rather than changing auxin biosynthesis or perception (Laplaze et al. 2007; Dello Ioio et al. 2007). It will be interesting to define at the molecular level how these hormones interact at various stages of vascular development. Recently, Mu¨ller and Sheen (2008) showed that an antagonist interaction between auxin and cytokinin was required for specifying the first root stem cell niche during early embryogenesis. Auxin antagonizes cytokinin output in the basal cell lineage by direct transcriptional activation of type A RESPONSE REGULATOR genes, ARR7 and ARR15, repressors of cytokinin signaling (Mu¨ller and Sheen 2008).
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Studies with tree species have indicated another hormone class, gibberellins, that control cambial activity (Fig. 2c). Application of gibberellins (GA) to decapitated tree stems promoted division and expansion of cambium cells, but, in contrast to auxin, exogenously applied GA had no effect on xylem differentiation. When auxin and GA were applied together a pronounced synergistic effect was observed (Digby and Wareing 1966). To re-evaluate earlier experiments and to uncover the crosstalk between auxin and GA in cambial growth, Bjo¨rklund et al. combined traditional apical feeding experiments with modern techniques to detect hormone concentration and gene expression. Interestingly, they found that feeding decapitated trees with auxin and GA together resulted in about a twofold increase of internal IAA levels compared with samples supplied with IAA alone. To test whether GA stimulates PAT they analyzed transcript levels of PttPIN1 and PttPIN2, which are known to be expressed in the cambium of poplar. Using reverse transcriptase PCR (RTPCR) they showed that GA stimulated PttPIN1 expression. Furthermore, they showed that auxin stimulates GA biosynthesis genes, inhibits GA degradation genes, and shares a common transcriptome with auxin (Bjorklund et al. 2007). Thus, crosstalk between auxin and GA seems to be required to regulate cambial activity. Pharmacological treatments with GA have shown that gibberellins are required for differentiation of xylem fibers and cell elongation of secondary xylem fibers (Digby and Wareing 1966, Warening 1958, Ridoutt et al. 1996). Besides affecting the longitudinal growth, GAs also can influence radial growth (Wang et al. 1997). GAs can increase cambial activity in trees, especially in conjunction with IAA. Transgenic hybrid aspen ectopically expressing a GA 20oxidase gene grew faster, both in terms of height and diameter. Thus, transgenic elevation of GA levels resulted in accelerated thickening of trees. It also affected secondary growth by increasing the number and length of xylem fibers. The increase of biomass was restricted to the shoot, as there was no difference between wild-type and transgenic trees concerning the root biomass (Eriksson et al. 2000). In addition to gibberellins, auxin, and cytokinins, ethylene has also been shown to affect secondary xylem development (Eriksson et al. 2000; Junghans et al. 2004). Ethylene and auxin crosstalk has important role in root elongation (Stepanova et al. 2007) and recent findings support that similar auxin–ethylene interaction occurs in secondary xylem development since ethylene biosynthesis genes are induced by auxin in wood-forming tissues (Nilsson et al. 2008). The Arabidopsis thickvein (tkv) mutant exhibits reduced auxin transport in the inflorescence stem, increased number of vascular cells (cambial, xylem and phloem), and hypersensitivity to exogenous cytokinin. The tkv mutation
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is located within the ACL5 gene, which encodes a putative spermine synthase and is expressed during vascular development in provascular cells and in procambial cells (Clay and Nelson 2005). ACL5/TKV is involved in vein definition (defining the boundaries between veins and nonvein regions) and in PAT, suggesting that polyamines may be involved in this process but the exact mechanism of their function is not known (Clay and Nelson 2005). It is important to emphasize that the vascular system is an integral component of the plant. Accordingly, it could be thought that other more global signals regulate the patterning or proliferation of the vascular system. Only recently it was shown that yet unknown flowering related signals from the shoot promote the late stage of cambial activity. Characteristic for the late stage of cambial activity is the excessive formation of secondary xylem as compared to secondary phloem (Fig. 2c; Sibout et al. 2008). Analyzing quantitative trait loci (QTL) of recombinant inbred lines (RIL) derived from a cross between the ecotypes Uk-1 and Sav-0 revealed that the major QTL controlling the xylem-to-phloem ratio in the hypocotyls coincided with the major flowering time QTL (Sibout et al. 2008). As FLOWERING LOCUS C (FLC), a major repressor of flowering (Baurle and Dean 2006), was a tightly linked candidate gene to this QTL, several RILs were analyzed for a possible correlation between xylem-to-phloem ratio, FLC expression, and flowering time. Indeed, low expression of FLC coincided with earlier flowering and high xylem-to-phloem ratio. However, analyzing secondary growth traits and flowering time in another RIL population revealed that the transition to flowering per se determines the phloem-to-xylem ratio rather than FLC alone. The idea that flowering triggers secondary xylem formation was further supported by the observation that ecotypes that flower very late did not show xylem expansion before flowering (Sibout et al. 2008). Furthermore, transiently inducing CONSTANS (CO), an activator of flowering (Putterill et al. 1995), can induce xylem expansion in the hypocotyls but does not seem to be the direct activator. Grafting either Sav-0 (expressing low FLC levels) or UK-1 (expressing high FLC levels) shoot stocks on Sav-0 root stocks revealed that a late flowering shoot inhibited the expansion of xylem in the root of an ecotype in which expansion of xylem would have already progressed (Sibout et al. 2008). It will be interesting to learn the molecular framework of this regulation.
Differentiation of conductive tissues During late embryogenesis and post embryogenesis further development in newly specified xylem and phloem domains of the vascular bundles results in differentiation of the vascular cell types. Both xylem cells (xylem
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parenchyma, xylem tracheary, and xylem fibers) and phloem cells (sieve elements, companion cells, and phloem parenchyma) differentiate in a spatially and temporally defined manner (Fig. 1). While xylem parenchyma cells and the phloem cells are living cells, xylem tracheary elements undergo developmentally controlled cell death to form hollow tubes. The observation that the frequency of tracheary element (TE) differentiation was dependent on the local cell density in Zinnia elegans mesophyll cell cultures (described above) suggested that the induction of transdifferentiation was induced by a diffusible factor, namely xylogen. Isolation of xylogen from the medium revealed that it is a 183-aa-long arabinogalactan protein (ZeXYP1) (Motose et al. 2001a, b, 2004). Double knockout mutants of the two Arabidopsis xylogen genes AtXYP1 and AtXYP2 showed discontinuous veination patterns in leaves, but did not result in complete loss of xylem. Based on these observations it has been concluded that xylogen is required for vascular development as a ‘‘mediator’’ of inductive signaling related to vascular development. As purified xylogen bound to stigmasterol and weakly to brassicasterol it was suggested that xylogen may function as a sterol-proteoglycan complex. As both auxin and cytokinins are required for TE differentiation Motose et al. examined their effects on the accumulation of xylogen. Auxin triggered the accumulation of the xylogen (ZeXYP1) transcript, whereas both auxin and cytokinins were required for the accumulation of xylogen protein. These observations suggest that a synergistic action of auxin and cytokinin is required to posttranscriptionally regulate the accumulation of xylogen in association with progression of the TE differentiation program (Fig. 2d) (Motose et al. 2004). So far only three genes have been described to be specifically involved in specifying xylem or phloem differentiation. Two NAC-domain transcription factors VND6 and VND7 have been identified as key regulators for specification of xylem identity. In the Arabidopsis root the central xylem axis consists of the early differentiating protoxylem adjacent to the pericycle and the later differentiating metaxylem in the central part of the xylem axis (Fig. 1). Both VND6 and VND7 are expressed during metaand protoxylem formation, respectively. Ectopic VND6 expression induced xylem differentiation with characteristics for metaxylem, whereas ectopic VND7 expression induced xylem differentiation with ultrastructural characteristics typical of protoxylem. To test whether plant hormones can modulate the expression of the two transcription factors, cultured hypocotyls were treated with auxin, cytokinin, and brassinosteroids. Application of auxin together with cytokinin was required to obtain ‘‘significant’’ expression, and treatment with all three hormones resulted in the highest expression of VND6 and VND7 (Fig. 2d)
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(Kubo et al. 2005). APL (ALTERED PHLOEM DEVELOPMENT), an MYB coiled-coil transcription factor, has been shown to be necessary, but not sufficient for the differentiation of sieve tube elements (SEs) or companion cells (CCs). In apl loss-of-function mutants neither SEs nor CCs develop, instead xylem vessels can be found at the usual positions for phloem cells. Ectopic expression of APL in the root tip suppresses differentiation of protoxylem but does not trigger formation of ectopic phloem cells (Bonke et al. 2003). It is not currently known whether APL is under control of hormonal regulation. The final step in xylogenesis is to form the waterconducting vessels. Tracheary elements undergo two distinctive specification processes: patterned secondary—wall formation and developmentally controlled cell death. Recently, three members of the NAC SECONDARY WALL THICKENING PROMOTING FACTORs (NST1, NST2, and NST3) and the SECONDARY WALLASSOCIATED NAC DOMAIN PROTEIN1 (SND1) have been shown to be key regulators of secondary wall formation (Mitsuda et al. 2005, 2007; Zhong et al. 2007). In Zinnia culture, Brassinosteroids have been shown to be one of the first signaling molecules upregulating genes that are involved in secondary-wall formation and the destruction of the cell. Thus, it was suggested that brassinosteroids trigger the entry into the final phase of differentiation (Yamamoto et al. 1997).
Future outlook Now that the major hormonal signaling pathways have been established, it is timely to approach the interactions of various growth regulators. Knowledge of the interactions between signaling molecules is still relatively scarce. One promising avenue for systematic mining of new interactions is provided by fluorescently labeled cell sorting combined with a global gene expression profiling approach, which has been used to establish a gene expression map during root development (Birnbaum et al. 2003; Lee et al. 2006; Brady et al. 2007). It will be interesting to see how these types of studies will eventually result in a genome-wide view of hormonal interactions during vascular development. Acknowledgments We thank Anthony Bishopp for critical reading of the manuscript. JD is supported by the European Molecular Biology Organisation (EMBO, ALTF 450-2007).
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