Signal Molecules Involved in Plant Embryogenesis

Plant Molecular Biology 26: 1305-1313, 1994. © 1994 Kluwer Academic Publishers. Printed in Belgium. 1305 Signal molecules involved in plant embryogenesis Ed D.L. Schmidt, Anke J. de Jong and Sacco C. de Vries* Department of Molecular Biology, Wageningen Agricultural University, Dreijenlaan 3, 6703 HA Wageningen, The Netherlands (* author for correspondence) Received 10 May 1994; accepted 11 May 1994 Key words: zygotic embryogenesis, somatic embryogenesis, chitinase, nod factor, signal molecules Abstract In plant embryogenesis, inductive interactions mediated by diffusable signal molecules are most likely of great importance. Evidence has been presented that at late globular stages in plant embryogenesis, perturbation of the polar auxin transport results in abberrant embryo morphology. Rhizobium lipo- oligosaccharides or Nod factors are a newly discovered class of bacterial molecules that are able to trigger initial steps in root nodule development in legumes. Part of the activity of Nod factors may be directed towards alteration of endogenous plant growth regulator balance. The same bacterial Nod factors promoted the formation of globular embryos in the carrot cell line ts 11. Whether there exist plant ana- logues of the Nod factors and whether these molecules are active as a more universal control system perhaps designed to initiate and or mediate gradients in auxin and cytokinin remains to be determined. Introduction is highly vacuolated. Dual fertilization of the dip- loid central cell and the haploid egg cell results in Currently there is a wide and increasing interest the endosperm and the zygote respectively. The in the molecular-genetic analysis of plant embryo- first zygotic division is asymmetrical and yields a genesis. Detailed descriptions of gametogenesis small apical cell and a large basal cell. The basal and embryogenesis have been the subject of cell remains positioned at the micropylar pole of many recent studies [1-8] as well as reviews the embryo sac, and undergoes a series of trans- [9-15] and therefore will only be recapitulated versal divisions to form the suspensor. From the briefly. uppermost cell of the suspensor, the hypophysial The male gametophytes or pollen grains are cell, the centre of the future root meristem is formed in the anther, while the female gameto- formed [17]. The apical cell undergoes three di- phyte or embryo sac is formed in the pistil. In visions, resulting in the octant stage embryo angiosperms that exhibit the polygonum type [ 16 ] proper. Tangential divisions then set apart the it consists of seven cells: the egg cell, two syner- protoderm cells, from which the epidermis is de- gids, the central cell and three antipodal cells. The rived. Development of the Arabidopsis embryo polarized egg cell and synergids are positioned at from fertilization, through the octant, globular, the micropylar pole of the embryo sac. The po- triangular, heart, torpedo and bent-cotyledon larity of the egg cell is reflected in the position of stages, to the mature desiccated embryo, has been the nucleus and most of the cytoplasm at the subdivided into a sequence of 20 different stages chalazal side of the cell, while the micropylar part [3]. [69] 1306 While the above-described developmental se- Signal molecules in zygotic embryogenesis quence that gives rise to the Arabidopsis embryo appears to involve a highly predictable series of Two mechanisms appear to be universally used in divisions, it is important to note that this is but animal embryogenesis to initiate cell differentia- one of the types of embryo development in plants tion. The first of these is a polarization of cellu- [ 16]. Many variations in the plants and positions lar determinants, sometimes, but not always, fol- of early cell divisions and in suspensor morphol- lowed by asymmetric cell division [29]. In plants, ogy have been described, with apparently little or fertilization is followed by an extensive redistri- no consequence for the eventual seedling mor- bution of organelles resulting in polarization of phology. Recently the systematic genetic dissec- the zygote. Asymmetric cell division occurs fre- tion of the formation of the zygotic embryo has quently in plants, and the analysis of the Arabi- been initiated [18-21]. Based on the mutant dopsis gnom mutant [30], in which the mutant phenotypes obtained, a division of the young em- phenotype appears correlated with the inability to bryo along the longitudinal axis into an apical, perform a normal unequal division of the zygote, central and basal region was proposed [20, 22]. clearly shows that this mechanism is indeed of A second, radial pattern, superimposed on the crucial importance in plant embryogenesis. The apical-basal pattern and consisting of the vascu- second mechanism consists of the interaction be- lar, ground and epidermal tissues, appears to be tween an inducing cell or tissue and a responding established independently. cell or tissue brought about by specific signal mol- Somatic or asexual embryogenesis is the pro- ecules. Signal molecules that are produced out- cess by which somatic cells develop into plants side of a group of equivalent cells are defined as through the same characteristic morphological inducers [ 31 ]. Cellular communication between stages as their zygotic counterparts. For dicots adjacent cells can occur by cell-surface-located these are the globular, heart and torpedo stages. signal molecules able to act as inducers. Cells that The ability to form embryos that do not orignate are not in direct contact with an inducer- from a fertilized egg cell is quite widespread producing cell can be influenced if the signal mol- among plants. It may occur naturally as in Mal- ecule is diffusable, usually resulting in a concen- axis, where somatic embryos form spontanously tration gradient. Signal molecules are defined as on the leaf tips [23], or in the form of apomictic morphogens when the slope of their concentra- processes [24]. Under in vitro conditions somatic tion gradient provides reference points for the embryos can either form directly on the surface of formation of a pattern. The local concentration of an organized tissue such as a leaf or stem seg- the morphogen then determines the response of ment, from protoplasts or from microspores, or the cells. indirectly via an intermediary step of callus or Caenorhabditis elegans has served as an ex- suspension culture [25]. By virtue of their excel- ample for the existence of a series of segregating lent experimental accessibility, somatic embryo- cytoplasmic determinants that result in a rigid cell genesis is exploited to isolate plant-produced lineage as a means to generate patterns in the molecules that have promotive effects on the for- embryo and differentiated cells later on in devel- mation of somatic embryos [26]. Both somatic opment [32]. Recently described mutants pro- embryogenesis as well as in vitro cultured zygotic vide evidence that a number of maternally ex- embryos are being employed to try and answer pressed genes that encode nuclear proteins and long-standing questions concerning the role of cell surface proteins similar to the lin-12 family 'classical' plant growth regulators such as auxin are involved in cell-inductive processes [33]. in embryogenesis [27, 28]. In plant development cell position rather than developmental history is considered to be essen- tial for the formation of the somatic tissues [34- 37 ]. This implies that cell-inductive processes and [70] 1307 the use of signal molecules that act at short range exhibit a fused collar-like arrangement of their and over longer distances might be important in cotyledon primordia, as opposed to the normal the organization of the plant embryo. However, bilateral arrangement [27]. Application of the no direct evidence is available that cell-inductive polar auxin transport inhibitor to excised and in processes are indeed occurring in plants. A se- vitro cultured zygotic embryos of Brassica resulted quential and transient expression of a plasma in a similar fused-cotyledon phenotype as ob- membrane arabinogalactan protein (AGP) served for the pin-1 mutant [27], and in the Ara- epitope, recognized by the monoclonal antibody bidopsis gnom mutant [30]. These results are in- JIM8, was observed in reproductive tissues and terpreted to suggest that polar auxin transport the suspensor of an early globular embryo of determines the transition from radial to bilateral Brassica. Pennell et al. [38] speculated that the symmetry in the globular dicot embryo. The amp-I JIM8 epitope may be a marker for a cell-inductive mutant [42], exhibiting an elevated level of cyto- process in plants. Whether AGPs themselves act kinins, has a complex and pleiotropic phenotype as signal molecules in zygotic embryogenesis is affecting photomorphogenesis and flowering time, not known. There is however some evidence from as well as an increase in the number of tricot and somatic embryogenesis (see next section) that tetracot seedlings. Multiplication of cotelydons is particular AGPs may indeed have a direct bio- also observed in embryo mutants of the hauptling logical function in embryogenesis. If so, they will type [15, 20]. It appears therefore that interfer- be likely to act as short-range inducer molecules ence with the local balance between auxin and over a distance of a few cells only. A fascinating cytokinin primarily influences the formation of result was recently reported for Fucus [39] where, the proper number and orientation of cotyledon upon laser microsurgery

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