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Shoot Meristem Formation and Maintenance Michael Lenhard and Thomas Laux*

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Shoot Meristem Formation and Maintenance Michael Lenhard and Thomas Laux* 44 Shoot meristem formation and maintenance Michael Lenhard and Thomas Laux* The shoot apical meristem of higher plants is a self-maintaining gests the existence of at least two ‘communication com- stem cell system which gives rise to the entire aboveground partments’ in the shoot meristem. Although it is not clear part of a plant. In the past year, genetic and molecular studies whether these compartments coincide with the classical have provided increasing insight into the processes of shoot CZ and PZ, an important conclusion of this work is that meristem formation and maintenance, as well as into the selective symplasmic coupling of cells could provide a relation between the apical meristem and its products. mechanism to restrict the spread of potential morphogens to separate regions in the shoot meristem. Addresses Lehrstuhl für Entwicklungsgenetik, Universität Tübingen, Auf der Clonal analyses in a number of plant species, including Morgenstelle 1, D-72076 Tübingen, Federal Republic of Germany Arabidopsis thaliana, provided evidence that all vegetative * e-mail: [email protected] and generative structures of the shoot are derived from one Current Opinion in Plant Biology 1999, 2:44–50 common set of stem cells [7–9]. These findings contradict the ‘méristème d’attente’ concept put forward by Buvat http://biomednet.com/elecref/1369526600200044 and colleagues some decades ago [10], which holds that © Elsevier Science Ltd ISSN 1369-5266 the germ cells are produced by a pool of stem cells set Abbreviations aside very early in development, similar to the germ line in CZ central zone animals. Recent clonal analysis in maize, however, has KAPP kinase-associated protein phosphatase taken up this concept again. The maize shoot meristem PZ peripheral zone forms a limited number of vegetative leaves before a ter- minal inflorescence, the tassel, is produced on the main Introduction axis. It was shown that the upper part of the tassel is One of the fundamental features of postembryonic devel- derived from a set of cells in the shoot meristem that does opment of higher plants is the reiterative formation of new not contribute to postembryonic vegetative growth, even if organs by the shoot meristem [1]. The shoot meristem is the extent of vegetative growth is artificially increased formed during embryogenesis and subsequently gives rise [11••]. The author concludes that some apical cells are set to internodes, leaves, axillery shoot meristems and flowers aside in the shoot meristem early in development to exclu- (Figure 1). The bases for this activity are the abilities of sively form tassel. This does not imply, however, that these the shoot meristem to: firstly, maintain a set of pluripotent cells become committed to the formation of the upper tas- stem cells in a central zone (CZ); secondly, to initiate sel early in development, rather that they could simply be organs from the progeny of the stem cells in a peripheral located in a position where they are not recruited during zone (PZ); and thirdly, to balance these two processes the vegetative phase of the maize shoot meristem. (reviewed in [2–5]). In the following review, we will dis- cuss papers of the past year with regard to four aspects: the Formation of the shoot meristem during organization of the shoot meristem; its formation during embryogenesis embryogenesis; the maintenance of an active shoot meris- The origin and development of the shoot meristem in tem in postembryonic growth; and finally the inter-relation the embryo have been discussed controversially between the shoot meristem and its products. (reviewed in [12,13]). On the basis of comparative mor- phology, it has been argued that when the shoot Organization of the shoot meristem meristem is first differentiated, the partitioning of the As stated above, the shoot meristem contains two cell pop- embryo apex simultaneously defines two regions of the ulations with distinct behaviors, that is, those in the center shoot meristem with separate functions, the cotyle- which remain pluripotent and those in the periphery which donary primordia at the periphery and the ‘apical initials contribute to organ formation and eventually differentiate. per se’ in the center, required for meristem perpetuation Thus, cell behavior must be co-ordinated within one pop- [13]. Kaplan concluded that the cotyledons represent the ulation and distinguished from that of the other first products of the shoot meristem, a view which is con- population, implying regulated intercellular communica- sistent with the observation that the shoot meristem tion. To address the question of whether specific specific gene SHOOTMERISTEMLESS (STM) [14] is cytoplasmic coupling is involved in this process, Rinne and only expressed in the central cells, and not in the pre- van Schoot microinjected fluorescent dyes into single epi- cursor cells of the cotyledons [13]. Recent molecular dermal cells of the birch shoot meristem and followed the studies of various genes implicated in embryonic shoot fluorescence spread [6••]. Intercellular coupling was meristem development, however, have demonstrated observed within a central and a peripheral region, but not that shoot meristem formation involves a succession of between these two regions, except for a transient period, events and that at the stage of cotyledon initiation not all possibly during the initiation of each new leaf. This sug- aspects are in place. Shoot meristem formation and maintenance Lenhard and Laux 45 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 Late heart stage Mature embryo Seedling whorl of organ primordia, the sepals (*). Scanning electron microscopy images. Inflorescence meristem * Floral meristems Expression analysis of the shoot meristem gene derived from genetic analysis [18] and with the proposed WUSCHEL (WUS) has indicated a considerably earlier role of the maize knotted1 (kn1) gene, a putative STM start of shoot meristem development than previously ortholog [19]. STM appears to be functional from early thought [15••]. WUS is expressed in the four inner apical stages on, since at least the expression of another meristem cells of the 16-cell embryo and through several asymmet- gene, UNUSUAL FLORAL ORGANS (UFO), requires STM ric cell divisions its expression segregates with a subset of activity as early as the late globular stage [17••]. daughter cells which become located in the center of the shoot meristem primordium (Figure 2). Mutant analysis In the heart stage embryo, when cotyledonary primordia indicated that WUS is only necessary for the development are apparent, expression of a further meristem gene, of the shoot meristem, but not for those cell lineages CLAVATA1 (CLV1), is initiated within the embryo apex derived from early WUS-expressing cells that contribute independently of STM activity (Figure 2 [17••]). Mutations to the cotyledons [16]. The function of WUS at very early in CLV1 result in a progressive enlargement of the meris- embryo stages, before a shoot meristem is evident, is tem during postembryonic development (see below). The unclear. One possibility is that WUS functions to preserve late onset of its expression in the embryo suggests, howev- a pluripotent state in the cells required later in the emerg- er, that CLV1 may not play a prominent role in very early ing shoot meristem. stages of shoot meristem development. By contrast, the PRIMORDIA TIMING (PT) gene affects meristem size at At the late globular stage, when the embryo consists of these stages. pt-mutations cause a progressive enlargement about 100 cells, expression of the STM gene is initiated of the shoot meristem region from the globular embryo (Figure 2, [17••]), and this step is independent of WUS stage onward, but this defect regresses during later plant activity at earlier embryo stages [15••]. STM is expressed in development [20•]. Consistent with the temporal differ- a central region of the embryo apex that may correspond to ence in the manifestation of the respective phenotypes, the apical cells per se as well as in cells separating the double mutant analysis suggests that PT and CLV1 func- cotyledon primordia [17••]. In its absence these cells dif- tion in two independent processes. ferentiate and fused organs are formed, suggesting that STM may keep these cells from participating in organ for- In zll mutants [21] (allelic to pinhead [22]), the cells in mation. This interpretation is consistent with models the shoot meristem primordium do not maintain STM 46 Growth and development Figure 2 Shoot meristem formation during Arabidopsis embryogenesis. The first indication of shoot Shoot meristem Shoot meristem development is the onset of Cotyledon WUS expression at the 16-cell stage, long before a shoot meristem is evident. Protoderm Subsequently, expression of STM and CLV1 Apical Hypocotyl is initiated. Initiation of STM expression is Basal independent of WUS activity and onset of CLV1 expression is independent of STM. The Root ZLL gene is necessary to maintain shoot meristem development at later embryo stages. Bars represent stages at which Zygote One-cell8-cell 16-cell Globular Heart Seedling mRNA is detected (WUS, STM, CLV1) or phenotypic defects are observed (ZLL). WUS Shaded regions in embryos represent approximate expression domains. STM CLV1 ZLL Current Opinion in Plant Biology expression and differentiate, indicating that ZLL is as Newman elegantly put it [26], raising the question of required to maintain the meristematic cell status in the how the identity of these cells is specified. In wus mutants, apex of the embryo [23••]. ZLL codes for a member of a stem cells appear to be mis-specified and to have differen- novel gene family, including ARGONAUTE1, a gene tiated [16].
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