Scientific Correspondence Zinnia. Everybody Needs Good Neighbors

Cells in an organism exist within a social context— the sum of interactions with neighboring cells help to define the nature of each individual. The Zinnia system provides a unique opportunity to study in vitro the interactions between different plant cell types and the consequences for commitment to a particular cell fate. Zinnia is a model system in which mesophyll cells, released from young leaves and incubated with auxin and cytokinin, become committed to a new cell fate. Up to 60% or so of the cells eventually transdifferentiate into dead lignified tracheary elements (TEs) over the course of about 4 d (Fukuda, 1996). The emphasis in past work has been on the TEs themselves, but it has become more evident of late that the system also provides a paradigm for studying cell-cell interactions in development, interactions that have been singularly difficult to approach before in plants. In this respect, animal systems have proven to be more amenable to experimental approaches, and the patterns of signaling between cells to determine cell fate are relatively well understood. The competence of animal cells to respond to extracellular signals, provided through paracrine, autocrine, or in the case of distant cells not of the same type, endocrine signaling mechanisms, depends on the prior developmental history of each cell. The polarity of the embryo permits the later patterning of broad domains in which the cell populations express different combinations of homeotic regulatory genes. These domains become progressively refined as groups of cells acquire positional information. Finally, individual cells become determined to specialized cell fates. In both animals and plants, developmental genetics has uncovered key regulatory genes that can broadly define cell fate. Additionally, in animals, experimental embryology has been used to establish the state of commitment to a particular cell fate by microsurgical manipulation of groups of cells into new environments and by observing whether they adopt the fate of their new or original environment. In plants, studies using genetic mosaics have shown that the position of a cell, not its clonal origin, determines its fate (Scheres, 2001). Rare cell division events place daughter cells in neighboring files in the Arabidopsis root. The fate of these daughters is appropriate to their new position (Kidner et al., 2000). Within meristems, cells transit through domains of expression of regulatory genes to their final fate, with only a small number of cells remaining uncommitted to provide a population of “stem” cells that renew the meristem continuously (Haecker and Laux, 2001). Although surgical excision and transplantation of specific cells is rarely feasible in intact plants, cell culture systems offer a useful and appropriate alternative. In particular, the Zinnia mesophyll cell system now offers an opportunity to study the consequences of extracellular signaling for developmental fate. Plant growth factors have been shown in two model systems to be involved in cell commitment. Ethylene is required for the final commitment of cells to produce a root hair in the Arabidopsis root epidermis (Tanimoto et al., 1995). Both mesophyll cells (Fukuda and Komamine, 1980) and epidermal cells (Church and Galston, 1989) of Zinnia elegans can be induced, by auxin and cytokinin, to transdifferentiate into TEs in vitro. Although Arabidopsis provides an excellent molecular genetic model, the Zinnia system has the advantage of being more amenable to biochemical or in vitro culture studies. Because differentiation is synchronously induced in a large number of the cells in a relatively homogeneous cell population, it is possible to study the biochemistry and molecular biology of xylogenesis free from the complexity of intact plant tissues (Fukuda, 1996; McCann, 1997). Three factors, wounding, auxin, and cytokinin, are involved in initiating TE formation in Zinnia. Mechanically isolated cells may be regarded as wounded cells, and wounding is known to induce TE formation in intact plants. When a vascular bundle in a stem is severed, a connection is reestablished by the transdifferentiation of intervening pith parenchyma into vascular elements (Sachs, 1981). However, many further signals are required to complete TE formation (Fukuda, 1996). Inhibitors of brassinosteroid synthesis block TE formation until a very late stage of differentiation (Yamamoto et al., 1997). Because the competence to differentiate is also highly dependent on cell concentration until a late stage of culture, this strongly suggests that cell-cell signaling mechanisms are involved and, therefore, that commitment and at 1 This work was funded by the Biotechnology and Biological Sciences Research Council and the Leverhulme Trust (grant no. F/00 255/A). * Corresponding author; e-mail [email protected]; fax 00 – 44-1603– 450022 www.plantphysiol.org/cgi/doi/10.1104/pp.010883.