The shoot apical meristem of higher plants is a self-maintaining stem cell system which gives rise to the entire aboveground part of a plant. In the past year, genetic and molecular studies have provided increasing insight into the processes of shoot meristem formation and maintenance, as well as into the relation between the apical meristem and its products.
Addresses
Lehrstuhl für Entwicklungsgenetik, Universität Tübingen, Auf der Morgenstelle 1, D-72076 Tübingen, Federal Republic of Germany *e-mail: [email protected]
Current Opinion in Plant Biology1999, 2:44–50 http://biomednet.com/elecref/1369526600200044 © Elsevier Science Ltd ISSN 1369-5266
Abbreviations CZ central zone
KAPP kinase-associated protein phosphatase
PZ peripheral zone
Introduction
One of the fundamental features of postembryonic devel-opment of higher plants is the reiterative formation of new organs by the shoot meristem [1]. The shoot meristem is formed during embryogenesis and subsequently gives rise to internodes, leaves, axillery shoot meristems and flowers (Figure 1). The bases for this activity are the abilities of the shoot meristem to: firstly, maintain a set of pluripotent stem cells in a central zone (CZ); secondly, to initiate organs from the progeny of the stem cells in a peripheral zone (PZ); and thirdly, to balance these two processes (reviewed in [2–5]). In the following review, we will dis-cuss papers of the past year with regard to four aspects: the organization of the shoot meristem; its formation during embryogenesis; the maintenance of an active shoot meris-tem in posmeris-tembryonic growth; and finally the inter-relation between the shoot meristem and its products.
Organization of the shoot meristem
As stated above, the shoot meristem contains two cell pop-ulations with distinct behaviors, that is, those in the center which remain pluripotent and those in the periphery which contribute to organ formation and eventually differentiate. Thus, cell behavior must be co-ordinated within one pop-ulation and distinguished from that of the other population, implying regulated intercellular communica-tion. To address the question of whether specific cytoplasmic coupling is involved in this process, Rinne and van Schoot microinjected fluorescent dyes into single epi-dermal cells of the birch shoot meristem and followed the fluorescence spread [6••]. Intercellular coupling was
observed within a central and a peripheral region, but not between these two regions, except for a transient period, possibly during the initiation of each new leaf. This
sug-gests the existence of at least two ‘communication com-partments’ in the shoot meristem. Although it is not clear whether these compartments coincide with the classical CZ and PZ, an important conclusion of this work is that selective symplasmic coupling of cells could provide a mechanism to restrict the spread of potential morphogens to separate regions in the shoot meristem.
Clonal analyses in a number of plant species, including
Arabidopsis thaliana, provided evidence that all vegetative and generative structures of the shoot are derived from one common set of stem cells [7–9]. These findings contradict the ‘méristème d’attente’ concept put forward by Buvat and colleagues some decades ago [10], which holds that the germ cells are produced by a pool of stem cells set aside very early in development, similar to the germ line in animals. Recent clonal analysis in maize, however, has taken up this concept again. The maize shoot meristem forms a limited number of vegetative leaves before a ter-minal inflorescence, the tassel, is produced on the main axis. It was shown that the upper part of the tassel is derived from a set of cells in the shoot meristem that does not contribute to postembryonic vegetative growth, even if the extent of vegetative growth is artificially increased [11••]. The author concludes that some apical cells are set
aside in the shoot meristem early in development to exclu-sively form tassel. This does not imply, however, that these cells become committed to the formation of the upper tas-sel early in development, rather that they could simply be located in a position where they are not recruited during the vegetative phase of the maize shoot meristem.
Formation of the shoot meristem during
embryogenesis
The origin and development of the shoot meristem in the embryo have been discussed controversially (reviewed in [12,13]). On the basis of comparative mor-phology, it has been argued that when the shoot meristem is first differentiated, the partitioning of the embryo apex simultaneously defines two regions of the shoot meristem with separate functions, the cotyle-donary primordia at the periphery and the ‘apical initials
per se’ in the center, required for meristem perpetuation [13]. Kaplan concluded that the cotyledons represent the first products of the shoot meristem, a view which is con-sistent with the observation that the shoot meristem specific gene SHOOTMERISTEMLESS (STM) [14] is only expressed in the central cells, and not in the pre-cursor cells of the cotyledons [13]. Recent molecular studies of various genes implicated in embryonic shoot meristem development, however, have demonstrated that shoot meristem formation involves a succession of events and that at the stage of cotyledon initiation not all aspects are in place.
Shoot meristem formation and maintenance
Expression analysis of the shoot meristem gene
WUSCHEL (WUS) has indicated a considerably earlier start of shoot meristem development than previously thought [15••]. WUSis expressed in the four inner apical
cells of the 16-cell embryo and through several asymmet-ric cell divisions its expression segregates with a subset of daughter cells which become located in the center of the shoot meristem primordium (Figure 2). Mutant analysis indicated that WUSis only necessary for the development of the shoot meristem, but not for those cell lineages derived from early WUS-expressing cells that contribute to the cotyledons [16]. The function of WUSat very early embryo stages, before a shoot meristem is evident, is unclear. One possibility is that WUSfunctions to preserve a pluripotent state in the cells required later in the emerg-ing shoot meristem.
At the late globular stage, when the embryo consists of about 100 cells, expression of the STM gene is initiated (Figure 2, [17••]), and this step is independent of WUS
activity at earlier embryo stages [15••]. STMis expressed in
a central region of the embryo apex that may correspond to the apical cells per se as well as in cells separating the cotyledon primordia [17••]. In its absence these cells
dif-ferentiate and fused organs are formed, suggesting that
STMmay keep these cells from participating in organ for-mation. This interpretation is consistent with models
derived from genetic analysis [18] and with the proposed role of the maize knotted1 (kn1) gene, a putative STM
ortholog [19]. STM appears to be functional from early stages on, since at least the expression of another meristem gene, UNUSUAL FLORAL ORGANS (UFO), requires STM
activity as early as the late globular stage [17••].
In the heart stage embryo, when cotyledonary primordia are apparent, expression of a further meristem gene,
CLAVATA1 (CLV1), is initiated within the embryo apex independently of STMactivity (Figure 2 [17••]). Mutations
in CLV1result in a progressive enlargement of the meris-tem during posmeris-tembryonic development (see below). The late onset of its expression in the embryo suggests, howev-er, that CLV1 may not play a prominent role in very early stages of shoot meristem development. By contrast, the
PRIMORDIA TIMING(PT) gene affects meristem size at these stages. pt-mutations cause a progressive enlargement of the shoot meristem region from the globular embryo stage onward, but this defect regresses during later plant development [20•]. Consistent with the temporal
differ-ence in the manifestation of the respective phenotypes, double mutant analysis suggests that PT and CLV1 func-tion in two independent processes.
In zll mutants [21] (allelic to pinhead [22]), the cells in the shoot meristem primordium do not maintain STM Figure 1
Development of the Arabidopsis shoot meristem. The shoot meristem (arrow) arises between the outgrowing cotyledonary primordia during embryogenesis. In the mature embryo, the shoot meristem (arrow) has initiated the first true leaf primordia (*). In seedlings, the shoot meristem forms a shallow dome and gives rise to leaves (*). The inflorescence meristem initiates floral meristems at its flanks. The oldest floral meristem (at right) has already formed the first whorl of organ primordia, the sepals (*). Scanning electron microscopy images.
Late heart stage Mature embryo Seedling
Floral meristems Inflorescence meristem
*
*
*
expression and differentiate, indicating that ZLL is required to maintain the meristematic cell status in the apex of the embryo [23••]. ZLLcodes for a member of a
novel gene family, including ARGONAUTE1, a gene involved in leaf development [24••], and sequences
derived from genomic sequencing projects, e.g. in humans and C. elegans. The recently cloned rabbit trans-lation initiation factor eIF2C turned out to be another member of this family [25], suggesting that ZLL and
AGO1 could be implicated in translational control. As mutations in ZLL result in specific defects, the gene could be involved in tissue- and/or stage-specific transla-tional control. ZLLis expressed in the vascular precursor cells underlying the shoot meristem primordium from earliest embryo stages on and in the embryo apex at later stages [23••]. In which cells its expression is needed for
meristem development remains to be determined. Interestingly, the requirement for ZLLin primary shoot meristem development is only transient. Once the first true leaf primordia are present, the shoot meristem appears to be able to self-maintain independently of ZLL
activity [23••].
Thus, from these studies it follows that shoot meristem formation is a prolonged, dynamic process which begins during early embryo pattern formation. Also, whereas some aspects of the formation of cotyledons are strikingly simi-lar to that of leaves, important differences should not be overseen, such as that not all molecular mechanisms of the postembryonic shoot meristem are in place when the cotyledons are initiated.
The shoot meristem in
postembryonic development
Clonal analysis indicated that stem cells of the shoot meris-tem are not permanent but are instructed by positional information as ‘temporary occupants of a permanent office’
as Newman elegantly put it [26], raising the question of how the identity of these cells is specified. In wusmutants, stem cells appear to be mis-specified and to have differen-tiated [16]. In contrast to stmmutations, however, cells in
wus apices are not recruited into organs, suggesting that
WUSpositively regulates cell fate rather than preventing organ formation. WUSwas cloned and shown to encode a putative homeodomain protein of a novel subtype [15••]. WUSis expressed in a small group of cells in the meristem center underneath the presumed position of the stem cells. A conceiveable model derived from these data is that
WUS-expressing cells act as an organizing center confer-ring stem cell fate to overlying neighbors (Figure 3). This model implies similarities in the organization of shoot and root meristems, since in the root meristem the stem cells also appear to be maintained by signaling from a central organizing cell group, the quiescent center [27••]
(Figure 4). Similarities between shoot and root meristem regulation have also been concluded from the study of the
Defective embryo and meristems (Dem) gene of tomato which affects cell divisions in both meristems [28•]. Because
organ primordia are also affected in the demmutant, how-ever, the significance of Dem for meristem development still needs to be determined.
Once the progeny of the stem cells have left the center of the shoot meristem, they are recruited into organogenesis and eventually differentiate. In Arabidopsis, this process is promoted by the CLVand MGOUN(MGO) genes.
CLV1, encoding a putative receptor kinase, and CLV3, which interacts genetically with CLV1, are likely to be com-ponents of a common signaling pathway, with mutations in either gene causing a progressive increase in meristem size [29,30]. Previously two mutually not exclusive models for their role had been proposed: CLV signaling could pro-mote the entry of cells into organogenesis and/or Figure 2
Shoot meristem formation during Arabidopsis
embryogenesis. The first indication of shoot meristem development is the onset of
WUSexpression at the 16-cell stage, long before a shoot meristem is evident. Subsequently, expression of STMand CLV1
is initiated. Initiation of STMexpression is independent of WUSactivity and onset of
CLV1expression is independent of STM. The
ZLLgene is necessary to maintain shoot meristem development at later embryo stages. Bars represent stages at which mRNA is detected (WUS, STM, CLV1) or phenotypic defects are observed (ZLL). Shaded regions in embryos represent approximate expression domains.
Apical Basal
Protoderm
Shoot meristem Cotyledon
Shoot
Hypocotyl
Root
8-cell 16-cell Heart Seedling
One-cell Globular
Zygote
ZLL WUS
STM
CLV1
negatively regulate the proliferation of meristem cells [29,31]. The latter alternative has recently been refuted by Laufs et al.These authors find that in clv3 meristems the size of the central region of low mitotic activity is increased and the cells in this region divide even less frequently than in wild type [32••]. Thus, it appears likely that the CLV
pathway primarily enhances the rate of a differentiation step during organ formation (Figure 3).
To gain first insight into how CLV signaling is processed within the cell, two laboratories examined the biochemi-cal properties of CLV1 and its interaction with the kinase-associated protein phosphatase KAPP [33••,34••].
The CLV1 intracellular domain can autophosphorylate and appears to oligomerize with and transphosphorylate other CLV1 molecules. KAPP was found to be able to dephosphorylate CLV1 in vitro and the results of trans-genic studies point at a role of KAPP as a negative regulator of CLV1 signaling in planta. As KAPP interacts with various receptor-like kinases similar to CLV1 [35], however, it may be a more general modulator of different receptor kinase pathways.
Mutations in the CLV2gene result in an increase of shoot meristem height and an extra whorl of organs in flowers, similar to weak clv1 and clv3 alleles [36•]. Organ
devel-opment is also affected in clv2, however; for example the pedicel length of flowers is increased compared to wild type. clv1and clv3are epistatic to clv2 with respect to flo-ral organ number, but additive with respect to pedicel length. This suggests that CLV2acts in the same pathway as CLV1/3 to regulate meristem activity, whereas it seems to affect further organ development independently. The initiation of lateral organs by the shoot meristem also requires the MGOUN(MGO) genes. mgo1and mgo2result in a reduction of the number of leaves and floral organs, larger meristems and fasciation [37•]. In contrast to clv3
(see above), mgo2 shoot meristems accumulate cells in the PZ [32••]. As clv3 mgodouble mutants are additive,
the genes appear to be involved in different steps of organ formation: whereas CLV3 affects the rate of the transition of cells from CZ to PZ, the MGO genes may affect the partitioning of PZ cells into organ primordia (Figure 3).
The maize homeobox gene kn1appears to counteract dif-ferentiation of meristem cells and organ formation [19]. Recent overexpression studies, however, are consistent with differences in the action of kn1as well as in the devel-opmental plasticity of leaf cells in monocotyledonous and dicotyledonous plants. Whereas overexpression of kn1 in tobacco produced ectopic meristems on leaves [38], no such effect has been observed in studies with transgenic maize [39•] and barley [40•]. In barley, the only effect of
ectopic expression of maize kn1was the formation of addi-tional florets on the awn of primary spikelets, suggesting that kn1 might have induced inflorescence meristem fate in cells of the normally determinate awn [40•].
In contrast to Arabidopsis,in some species the shoot meris-tem only forms an intrinsically limited number of structures. How is the meristem program terminated in such species? One example is the maize spikelet meristem which gives rise to two floral meristems only. Mutations in the indeterminate spikelet1 (ids1) gene abolish spikelet meristem determinacy such that it gives rise to additional floral meristems, indicating a role of ids1in meristem ter-mination. Chuck et al.showed that ids1 codes for a gene related to APETALA2, which is required in Arabidopsis
flower development [41••]. Although the precise
regulato-ry mechanism for spikelet meristem determinacy is unknown, one attractive hypothesis is that idsacts as a neg-ative regulator of those factors necessary for maintaining indeterminacy, such as kn1.
The relationship between the shoot meristem
and leaves
Is the shoot meristem autonomous and independent from its products, or is there a mutual interaction between shoot meristem and organs? The latter view is supported by clas-sical studies demonstrating that continued activity of the shoot meristem depends on hormonal supply from young leaf primordia [42]. Recent studies on mutations primarily affecting leaf development point into the same direction. The phantastica(phan) mutation of Antirrhinumpartly dis-rupts dorsoventrality of lateral organs, with ventral (abaxial, lower leaf side) tissue present on the upper side of leaves, and blocks the outgrowth of leaf primordia [43••]. The gene Figure 3
Genes involved in the regulation of shoot meristem activity. WUS
expression in the basal part of the central zone (CZ) affects the state of the overlying stem cells. The CLVsignaling pathway, including
CLV1and CLV3, promotes a differentiation step reflected by the transition of cells from the CZ to the PZ. This step is counteracted by
STMin Arabidopsis, and the maize kn1possibly plays a similar role. The MGO genes promote formation of organ primordia (p) from cells of the PZ. Expression of the PHANgene in leaf primordia is required for maintenance of shoot meristem activity. The figure combines data from Arabidopsis(WUS, STM, CLV, MGO), Antirrhinum(PHAN) and maize (kn). See text for details. sc, stem cells; RZ, rib zone.
RZ
PZ CZ
PZ
p sc
p
CLV MGO STM/kN1
(PHAN)
Current Opinion in Plant Biology
codes for a putative MYB transcription factor and is expressed uniformly in young primordia of leaves and floral organs. When the formation of leaves is disrupted in condi-tional phan alleles, shoot development discontinues, indicating that leaf development is required for shoot meris-tem activity (Figure 3). The dominant phabulosamutation of
Arabidopsisaffects leaf development in a manner opposite to that of phantastica, causing a transformation of ventral into dorsal (adaxial, upper leaf side) leaf tissue to varying degrees [44••]. Interestingly, in such dorsalized leaves, ectopic
meristems are formed opposite to the leaf axils, at the lower side of the petiole base, indicating a correlation between dorsal leaf fate and the development of axillary shoot meris-tems and as the authors put it, “a cyclical model for shoot development: the shoot meristem makes leaves which in turn are responsible for generating new shoot meristems”.
Conclusions
The literature reviewed provides new insights into the mechanisms underlying the formation and maintenance of the shoot meristem. Several interesting new mutants have been identified and several genes have been isolated that will considerably add to our understanding of these process-es. Nevertheless, despite extensive screens by several laboratories, the number of regulators specific for shoot meristem development that have been identified appears small. Finding further novel components may require spe-cific screening strategies, as exemplified by the isolation of suppressors of the clv1mutation [45]. With several impor-tant genes cloned which are involved in the regulation of meristem cell fate and organ formation, the important ques-tions can now be addressed of what is their cellular function, which genes and processes are their targets and how are their functions integrated in an active shoot meristem.
Acknowledgements
We gratefully acknowledge support from grants by the Deutsche Forschungsgemeinschaft to Thomas Laux and by a stipend from the Boehringer Ingelheim Fond to Michael Lenhard. We thank the member of the Laux laboratory for helpful comments on the manuscript. We apologize to those colleagues working in the field whose work was not mentioned due to space constraints.
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest ••of outstanding interest
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Figure 4
Model for the maintenance of stem cells in shoot and root meristems. Analysis of the
WUS gene and cell ablation studies allow for a model in which maintaining the state of stem cells (lightly shaded) in shoot and root meristems requires information (white arrows) from neighboring cell groups (darkly shaded), theWUS expressing cells and the quiescent center (QC), respectively. Progeny of the stem cells in the surrouding regions (white areas) undergo differentiation, presumably integrating information (shaded arrows) from more mature tissues (for review see [2]). CZ, central zone; crc, central root cap; lrc, lateral root cap; p, leaf primordia; PZ, peripheral zone; RZ, rib zone.
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• expression of the maize kn1gene phenocopies the Hooded
mutant of barley.Development1997, 124:3737-3745.
Constitutive expression of maize kn1in barley results in ectopic flowers, a defect similar to that of the Hoodedmutation of barley. Notably, no ectopic shoot meristem formation is observed, as it has been reported in overex-pression studies in tobacco.
41. Chuck G, Meeley RB, Hake S: The control of maize spikelet
•• meristem fate by the APETALA2-like gene indeterminate spikelet1.Genes Dev1998, 12:1145-1154.
This paper describes the cloning and analysis of the indeterminate spikelet1
gene, that is required for determinacy of the first two branches (spikelets) of the maize inflorescence. The possible implications of ids1for inflorescence architecture in other grass species are discussed.
42. Shabde M, Murashige T: Hormonal requirements of excised
Dianthus caryophyllusL. shoot apical meristem in vitro. Am J Botany1977, 64:443-448.
43. Waites R, Selvadurai HR, Oliver IR, Hudson A: The PHANTASTICA
•• gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum.Cell1998,
93:779-789.
The PHANgene, required for leaf dorsoventrality, was cloned and shown to encode a putative MYB transcription factor. Its expression pattern and the mutant phenotype suggest a role in the specification of leaf identity. PHAN
is necessary for sustained meristem activity in a non-cell-autonomous man-ner, reinforcing the observation that shoot meristem activity is affected by signaling from leaves.
44. McConnell JR, Barton MK: Leaf polarity and meristem formation in
•• Arabidopsis.Development1998, 125:2935-2942.
The dominant phb-dmutation which disrupts dorsoventrality of lateral organs leads to the ectopic formation of axillary meristems on the lower side of leaf petioles. This interesting effect suggests that dorsal (adaxial) leaf fate pro-motes the formation of axillary shoot meristems.
