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. Apical Meristems . Cell Cycle Control in Meristems
Apical Meristems
The true vegetative shoot apical meristem (SAM) comprises a relatively small population of cells above the youngest primordium varying from as few as 50 cells in Arabidopsis thaliana to over 1000 in Chrysanthemum segetum. This cell population conforms to an apical dome, which can be pronounced in some species (e.g. Lolium temulentum) but attened in others (e.g. Helianthus annuus). Apical dome size varies between species (Table 1); the basal diameter of the dome can vary from 50 to 3000 mm (Mauseth, 1991). However, in the 250 000 angiosperms worldwide, there will probably be some that exhibit larger apical domes than indicated in Table 1. A vegetative SAM changes size constantly. Through cell division, it increases to a threshold size large enough to partition itself into a smaller dome, primordia and subapical tissue (Figure 1). The interval between the initiation of successive primordia is dened as the plastochron. The process will be repeated in a semiiterative fashion because, during vegetative growth, the plastochron tends to lengthen; this, in turn, is reected in dierent growth rates between successive plastochrons (Lyndon, 1977). Notably, the apical dome cells exhibit exponential cell cycle kinetics so that dome growth during successive plastochrons can be expressed as sawtooth plots when temporal increases in cell number are plotted on a loge scale. Vegetative SAMs are described in at least three dierent ways: according to planes of division (Tunica Corpus theory), according to cell fates (L1, L2, L3) or according to cell size/rates of cell division (zonation). The Tunica Corpus theory (Schu epp, 1917) supports the partitioning of cells into domains according to their plane of cell division. In the tunica, cells divide with the plane of chromosome separation at anaphase parallel to the surface
Table 1 Sample of vegetative apical domes ranked in order of increasing size (for a review, see Francis, 1997) Plant Arabidopsis thaliana Helianthus annuus Silene coeli-rosa Chrysanthemum segetum Diameter of vegetative apical dome (mm) 50 70 100 1400
(anticlinal). Typically the tunica is conned to the outer cell layers. In the corpus, cells divide in any plane and this domain is inside the tunica. Most dicotyledonous apical domes exhibit a tunica of two to four layers. When there are two tunica layers they are often described as L1 and L2, with L3 representing the outermost layer of corpus. As mentioned above, leaves are initiated from the apical dome. Fate maps of leaves often indicate plasticity because cells in a particular leaf tissue may be derived from all three layers, but sometimes only from L1 and L2. In other words, cell layers of the apical dome might be best regarded as sources of cells, while fate is imposed on them through positional controls during development (Lyndon, 1998). On the basis of cell size and rates of cell division, dierent regions of the dome can be classied in dierent zones: a central zone (CZ) of large slowly dividing cells, a peripheral zone (PZ) of smaller, faster dividing cells and a pith-rib meristem (PRM) of cells with intermediate size and an intermediate rate of cell division relative to the CZ and PZ ` de, 1967). Leaf primordia arise on the side of the (Nougare dome from cells of the PZ, which, as explained above, can include L1, L2 and L3 layers. In the garden pea, the primordium begins as a cohort of periclinal cell divisions (plane of anaphase separation at 908 to the surface) within the PZ occurring about one-third of the way through a plastochron (Lyndon, 1970). In general terms, leaf initiation is a function of both the plane of cell division in the PZ coupled with changes in the elasticity of the cell walls of the epidermal cells at the point of primordium outgrowth (Green, 1994). However, the primary signal for leaf primordium initiation has yet to be discovered. At the end of each plastochron, part of the PRM is partitioned into the subapical region. Within this region are the progenitor cells for both the internode and node although it is impossible to resolve these tissues at this early stage (Figure 1). Recent studies of mutants of Arabidopsis, which are decient in normal SAM function, have led to the discovery of genes that regulate vegetative development. For example, the shootmeristemless (stm) mutant of Arabidopsis is virtually unable to form a shoot meristem and is regarded as a more severe mutation than the socalled topless (tpl) mutant, which is also unable to form a shoot meristem (Evans and Barton, 1997). SHOOTMERISTEMLESS (STM) encodes a KNOTTED1-type of homeodomain protein, which is rst detected in one to two
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ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net
Apical Meristems
Figure 1 Median longitudinal section of a shoot apical meristem of the grass, Dactylis glomerata. A is the apical dome; B is the subapical region containing the new leaf primordium as a bump on the left side adjacent to a central region in which the progenitor cells of the node and internode are located. Bar, 100 mm.
cells of the late globular stage of embryogenesis. First discovered in maize, mutations in KN1 result in knots of tissue forming around veins of the leaf blades (reviewed by Evans and Barton, 1997). A consensus view is that STM is a transcription factor regulating the expression of other genes, including TPL. Another target gene is WUCHSEL, which is required for cell identity in the centre of the SAM. This gene cascade is essential for normal SAM morphogenesis (Evans and Barton, 1997). STM also has important interactions with CLAVATA1(CLV1), the expression of which can regulate the number of cell layers within the meristem. One idea was that STM:CLV1 could regulate cell fates in the meristem (Laux and Shoof, 1997). Root apical meristems are located in the tips of roots and can comprise between 125 000 and 250 000 cells spanning approximately 2 mm of apical tissue. Root apical meristems exhibit specic tissue domains. At the centre is the central stele, surrounded by the cortex, which is in turn surrounded by the epidermal layer. Classically, these three layers correspond to Hansteins (1870) histogens: the periblem, plerome and dermatogen, which were perceived as discrete domains of founder cells for each tissue. These terms were originally applied to shoot apices but the plerome and periblem are not easily distinguishable in SAMs. Strictly speaking, the RAM is subapical in that it is protected by a root cap, thus invoking Hansteins fourth histogen, the calypterogen. Hence, the RAM gives rise to cells of the various tissue domains, including the root cap. The histogens were shown to be less specic in terms of
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tissue-organizing ability by F. A. L. Clowes at Oxford, who predicted, and subsequently discovered, a population of cells at the pole of the various tissue domains that divided much more slowly than surrounding cells (Clowes, 1954, 1956). This was the quiescent centre (QC), which led Clowes to develop a theory of root growth based on apical initials displaced from the QC by cell division, which then surround the quiescent centre. Central to this theory was that the apical initials themselves have no set fate but give rise to descendants, which then establish the tissue domains (Clowes, 1967). The cells of the QC are stimulated into more rapid cell division by decapping, tissue damage or by radiation leading to regeneration of the lost parts (Clowes, 1970). Hence, QC cells would conform to a population of founder cells (Barlow, 1997). More recently, Scheres and colleagues in Utrecht, using laser ablation on roots of Arabidopsis, have demonstrated that QC cells exert a negative regulation of cell dierentiation on surface contacting apical initials. These observations conformed to a hypothesis whereby QC cells repress the dierentiation of contacting apical initials, enabling the latter to divide (van den Berg et al., 1997). Clearly, the frequency of cell division is highest in the RAM and SAM of the plant. At the margins of the RAM, cells are left behind to elongate and dierentiate. Thus, at this boundary region, the meristem is exhibiting steadystate cell cycle kinetics, where a cell division at the periphery of the meristem results in one cell elongating while the other remains part of the proliferative pool. This
ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net
Apical Meristems
helps to explain how the RAM remains fairly constant in size during root growth, whereas the SAM is constantly changing size (see above).
lateral root initiation requires the expression of a newly discovered cyclin, cycd4At (De Veylder et al., 1999). SAMs exhibit gradients of cell division, slowest in the CZ, fastest in the PZ and intermediate in the PRM. For example, in Chrysanthemum at 208C, cell cycle times for the CZ, PZ and PRM were 139, 48 and 70 h, respectively ` de, 1977). Clearly, Cdk activity is (Rembur and Nougare high in SAMs but the mechanism for spatial regulation of cell division is unknown. However, it is anticipated that there will be links between genes that regulate development and those that control the cell cycle. One clue in this direction was the nding that a gene that is essential for megagametophyte and embryo development, PROLIFERA, encodes a minichromosome maintenance (MCM)like protein; MCMs are important regulators of DNA replication (Springer et al., 1995). Integration of the data is shedding light on the way that extracellular growth factors impinge on the cell cycle. For example, gibberellic acid treatment can lead to the upregulation of Cdc2 in rice and cytokinins can inuence the activation of Cdc2 in the garden pea (for a review, see Francis and Sorrell, 2000). Over the next few years it is anticipated that Cdkcyclin interactions will be veried in plants and that signal transduction chains mediated by plant growth regulators that interface with cell cycle control will be resolved, as will some of the links between developmental genes and cell cycle genes. Integration of the data on such interactions will be important in understanding cell cycle regulation in meristems during higher plant development.
References
Barlow PW (1997) Stem cells and founder zones in plants, particularly their roots. In: Potten CS (ed.) Stem Cells, pp. 2958. London: Academic Press. Clowes FAL (1954) The promeristem and the minimal construction centre in grass root apices. New Phytologist 53: 108116. Clowes FAL (1956) Localisation of nucleic acid synthesis in root meristems. Journal of Experimental Botany 7: 307312. Clowes FAL (1967) The quiescent centre. Phytomorphology 17: 132140. Clowes FAL (1970) The immediate response of the quiescent centre to Xrays. New Phytologist 69: 118. Cockcroft CE, den Boer BGW, Healy JM and Murray JAH (2000) Cyclin D control of growth rate in plants. Nature 405: 575579. De Veylder L, Almedia Engler J de, Burssens S et al. (1999) A new D-type cyclin of Arabidopsis thaliana expressed during lateral root formation. Planta 208: 453462. Evans MS and Barton MK (1997) Genetics of angiosperm shoot apical meristem development. Annual Review of Plant Physiology and Plant Molecular Biology 48: 673701. Francis D (1997) The stem cell concept applied to shoot meristems of higher plants. In: Potten CS (ed.) Stem Cells, pp. 5974. London: Academic Press. Francis D and Sorrell DA (2001) The interface between the cell cycle and plant growth regulators: a mini review. Plant Growth Regulation (in press). Gonthier R, Jacqmard A and Bernier G (1987) Changes in cell cycle duration and growth fraction in the shoot meristem of Sinapis alba during oral transition. Planta 170: 5559.
ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net
Apical Meristems
Green PB (1994) Connecting gene and hormone action to form, pattern and organogenesis: biophysical transductions. Journal of Experimental Botany 45: 17751788. Hanstein J (1870) Die Entwicklung des Keimes der Monokotylen und der Dikotylen. Botanisch Abhandlen 1: 1112. Hemerly AS, Ferreira P, de Almeida J et al. (1993) cdc2a expression in Arabidopsis is linked with competence for cell division. Plant Cell 5: 17111723. Kinsman EA, Lewis C, Davies MS et al. (1997) Elevated CO2 stimulated cells to divide in grass meristems: a dierential eect in two natural populations of Dactylis glomerata. Plant, Cell and Environment 20: 13091316. Laux T and Shoof H (1997) Maintaining the shoot meristem the role of CLAVATA1. Trends in Plant Science 2: 325328. Lyndon RF (1970) Planes of cell division in the shoot apical meristem of Pisum. Annals of Botany 34: 1928. Lyndon RF (1977) Interacting processes in development at the shoot apex. Society for Experimental Biology Symposium 31: 221250. Lyndon RF (1998) The Shoot Apical Meristem. Cambridge: Cambridge University Press. Mauseth JD (1991) Botany. Orlando, FL: Holt Rhinehart & Winston. Mironov V, De Veylder L, Van Montague M and Inze D (1999) Cyclindependent kinases and cell division in plants the nexus. Plant Cell 11: 509521. Norbury C and Nurse P (1992) Animal cell cycles and their control. Annual Review of Biochemistry 61: 441470. ` de A (1967) Experimental cytology of the shoot apical cells Nougare during vegetative growth and owering. International Review of Cytology 21: 203351. ` de A (1977) Duration of cell cycles in the shoot Rembur J and Nougare apex of Chrysanthemum segetum L. Zeitschrift fur Panzephysiologie 81: 173179.
Scherr CJ (1996) Cancer cell cycles. Science 274: 16721677. Schu epp O (1917) Untersuchungen uber Wachstum und Formwechsel von Vegetationspunkten. Jahrbuche fu r Wissenschaften Botanisch 57: 1779. Soni R, Carmichael JP, Shah ZJ and Murray JAH (1995) A family of cyclin D homologues from plants dierently controlled by growth regulators and containing the conserved retinoblastoma interaction motif. Plant Cell 7: 85103. Springer PS, McCombie WR, Sundaresen V and Matienssen RA (1995) Gene trap tagging of PROLIFERA, an essential MCM2-3-5-like gene in Arabidopsis. Science 268: 877880. van den Berg C, Willemsen V, Hendriks G, Weisbeek P and Scheres B (1997) Short-range control of cell dierentiation in the Arabidopsis root meristem. Nature 390: 287289.
Further Reading
Francis D, Dudits D and Inze D (1998) Plant Cell Division. London: Portland Press. Lyndon RF (1998) The Shoot Apical Meristem. Cambridge: Cambridge University Press. Meyerowitz EM (1997) Genetic control of cell division patterns in developing plants. Cell 88: 299308. Taiz L and Zeiger E (1998) Growth development and dierentiation. In: Plant Physiology, 2nd edn, chap. 16. Sunderland, MA: Sinauer Associates. Wolpert L (1998) Plant development. In: Principles of Development, chap. 7. Oxford: Oxford University Press.
ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net