View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Cell, Vol. 81, 467-470, May 19, 1995, Copyright 0 1995 by Cell Press Axis Formation Minireview in Plant Embryogenesis: Cues and Clues Gerd Jiirgens focus on pattern formation in the embryo that establishes Lehrstuhl fur Entwicklungsgenetik the basic body organization of flowering plants. Universitat Ttibingen The Shoot Me&tern: Linking Up the Embryo D-72076 Tiibingen with the Flower Federal Republic of Germany Pattern formation in animals is largely confined to em- bryogenesis such that the future adult form is represented in the body organization of the mature embryo. By con- Imagine a textbook entitled Developmental Biology that trast, plant embryogenesis produces a juvenile form, the focuses entirely on plants, mentioning animals only for seedling, that lacks most structures of the adult plant. Em- their peculiar way of making germ cells by setting aside bryogenesis in essence organizes two groups of stem cells a group of precursor cells early in the embryo. The con- at the opposite ends of the body axis, the primary meri- verse has been, and still is, common practice. It is true stems of the shoot and the root. These meristems then that the regenerative potential of plants, which is indeed add new structures to the seedling, thus generating the impressive, sets them apart from the more familiar animal species-specific adult form during postembryonic devel- models: individual cells can give rise to embryos in culture; opment (Steeves and Sussex, 1989). Regardless of the localized groups of stem cells called meristems make the appearance of the adult plant, the shoot meristem is orga- adult plant in a seemingly autonomous fashion not only nized essentially the same way in different plant species. during normal development, but also by regeneration from Two functional units can be distinguished within the meri- lumps of undifferentiated cells in culture. These special stem: a central zone, which is required for self-renewal features notwithstanding, plants do develop from a fertil- and integrity of the meristem, and a peripheral zone, which ized egg cell, the zygote, during the normal course of their makes primordia of lateral organs and their associated life cycle and, like animals, have to establish thecharacter- secondary shoot meristems, such as leaves and flowers istic body organization of the multicellular adult form. Are (Steeves and Sussex, 1989). Whether leaves or flowers the underlying mechanisms the same or different? In the are produced depends on the physiological state of the past few years, the genetic and molecular analysis of meristem. In embryonic flower (emf) mutant seedlings, for flower development in two plant model species, Arabi- example, the primary shoot meristem skips the vegetative dopsis and Antirrhinum (snapdragon), has established a phase of making leaves altogether, producing flowers di- network of MADS domain transcription factors and others rectly (Sung et al., 1992). Shoot meristem identity seems that regulate this best-characterized process in plant de- to be conferred by the continuous expression of genes like velopment (Weigel and Meyerowitz, 1994). However, the maize homeobox gene Knotted7 (Knl), whose ectopic flower development is like putting the finishing touches expression can cause the formation of shoot meristems on the adult plant and may thus not give clues to mecha- on leaves (Sinha et al., 1993; Jackson et al., 1994). A nisms that underlie earlier processes such as axis forma- putative Arabidopsis homolog of Knl, the SHOOT MEW tion and the generation of the overall body organization. By STEM-LESS (STM) gene, is required for shoot meristem drawing largely on recent genetic studies in Arabidopsis, I formation both in the embryo and during regeneration from will briefly discuss postembryonic development that even- tissue culture (Barton and Poethig, 1993). How the activity tually culminates in the formation of flowers, but mainly of such shoot meristem-specific genes is established and Figure 1. Formation of the Apical-Basal Axis in the Arabidopsis Embryo (A) Asymmetric division of the zygote, giving a a proE small apical (a) and a large basal (b) cell. (B)The8-cellstage.Theproembryo(proE)con- sists of two tiers each of four cells (regions marked A for apical and and C for central) and b sus is connected to the extraembryonic suspensor (sus) via the founder cell of the basal region (B) of the embryo. I- (C) Embryo at heart stage. Approximate loca- tions of cell groups that give rise to the primor- dia of seedling structures are indicated. (D) Embryo at Torpedo stage. Clonal bound- aries are marked by thibk lines. The broken line indicates the upper end of the embryonic root derived from the root meristem initials (RMI). A B C D Below the quiescent center (QC) of the root meristem are the initials of the central root cap (CRC). Primordia of seedling structures: COT, cotyledons; HY, hypocotyl; ER, embryonic root; RM, root meristem; SM, shoot meristem. Cdl 466 maintained properly is not known. However, there are can- mainder of the root meristem, comprising the quiescent didate genes in Arabidopsis for performing these func- center and the initials of the central root cap. Data from tions. For example, the ZWLLE (ZLL) gene is specifically clonal analysis support the view that cell ancestry does involved in establishing the primary shoot meristem in the not play a role in generating apical-basal pattern ele- embryo but not in any other (nonembryogenic) context ments: clone boundaries are variable and, moreover, can (Jtirgens et al., 1994). Mutations in another gene, CLA- run across specificseedling structures, such as thecotyle- VATAl (CLW), cause overgrowth of primary and second- dons or the root meristem (Scheres et al., 1994; Dolan et ary shoot meristems that also results in the formation of al., 1994). Furthermore, the regularity of cell divisions in one or more supernumerary whorls in the center of the the early embryo is deceptive since mutations in the FASS flower (Clark et al., 1993). This phenotype suggests that (FS) gene totally alter the pattern of cell division, without the organization of the meristem is altered, owing to an affecting pattern formation (Torres Ruiz and Jiirgens, enlargement of the central zone required for self-renewal. 1994). Thus, the apical-basal pattern elements appear to Although more genes need to be identified to clarify this be established by cellular interactions in a position- point, it is conceivable that the primary shoot meristem dependent manner. may acquire a specific organization in the embryo that is What is the significance of the early regions along the subsequently maintained by cellular interactions within apical-basal axis? Evidence comes from the embryonic the meristem. phenotypes of mutations in three genes, MONOPTEROS Pattern Formation in the Arabidopsis Embryo (MP), FACKEL (FK), and GURKE (GK), which delete spe- The primary meristems of the shoot and the root originate cific seedling structures (Mayer et al., 1991). In mp em- at distinct positions in the embryo as part of the overall bryos, the cells in the central and basal regions divide body organization of the seedling (Barton and Poethig, abnormally, resulting in the absence of hypocotyl, root, 1993; Dolan et al., 1993). The latter may be viewed as the and root meristem (Berleth and Ji.irgens, 1993). In fk em- superimposition of an apical-basal pattern along the main bryos, the central region is affected while the basal region body axis and a radial pattern perpendicular to this axis. is not; in the seedling, the hypocotyl is missing such that The apical-basal pattern consists of a top-to-bottom array the cotyledons are directly attached to the root (Mayer et of elements: shoot meristem, cotyledons (embryonic al., 1991; Jiirgens et al., 1994). Since the root meristem leaves), hypocotyl (embryonic stem), radicle (embryonic is composed of cells from both the basal and the central root), and root meristem. The radial pattern is made up of regions, the basal region appears to induce the adjacent concentric rings of tissue layers: epidermis, ground tissue cells of the central region to become root meristem initials (cortex and endodermis), and vascular tissue (pericycle, that in turn produce the meristemderived embryonic root xylem, and phloem). The origins of the apical-basal and (see Figures 1 C and 1 D). A similar argument can be made radial pattern elements have been traced back to cell for the cotyledons, which are derived from both the apical groups of the early embryo in Arabidopsis where the very and the central regions. The phenotype of gk mutants is regular patterns of cell division facilitated these analyses essentially complementary to mp: the apical region of the (Mansfield and Briarty, 1991; Jiirgens and Mayer, 1994). embryo is altered, and, later on, gk seedlings lack shoot Formation of the Apical-Basal Axis meristem and cotyledons (Mayer et al., 1991). This sug- Apical-basal pattern formation starts with the asymmetric gests that the cotyledons are initiated within the apical division of the zygote that gives two daughter cells of un- region, which then signals to adjacent cells of the central equal sizes and different fates (Figure 1). The small apical region to participate in cotyledon formation. Thus, the cell generates, by cleavage divisions, an 8-celled proem- early regions may define genetically distinct groups of cells bryo that will give rise to most of the embryo. The large (compartments?) that generate the apical-basal pattern basal cell produces a file of 7-9 cells, of which all but the by cellular interactions. uppermost one will form the extraembryonic suspensor; How are the early regions established along the apical- the uppermost cell (hypophysis) joins the proembryo later basal axis? The boundary separating the central from the to give rise to part of the root meristem.