Differentiation and Development

Mitotic cell division in unicellular organisms such as bacteria or yeast produces identical sister cells that are also identical to the mother cell. But in multicellular plants, sister cells are different from each other and usually also from the mother cell that produced them. These differences result from variations of gene expression in cells that are genetically identical. (The alternative hypothesis, that differentiation depends on differences in gene content in different cell types, can be discounted because differentiated cells isolated from the plant and placed in sterile culture on suitable nutrient medium regenerate entire plants that contain all the expected cell types.) The fifty or so specialized cell types of higher plants result from the operation of three developmental processes: cell polarity, asymmetric cell divisions, and positional information.

Origin of Cell Polarity

Polarity is the condition in which opposite ends of a structure are different. In biology this can apply to a cell or a tissue or an organism. Polarity in a multicellular plant exists in the first cell, the zygote , with the consequence that the two sister cells produced by the first division have different developmental fates.

The best studied example is the origin of polarity in the zygote of Fucus, a brown alga of the marine intertidal zone. Eggs are released into the seawater and fertilized. Polarity is established initially by the site of sperm penetration, and in the absence of other disturbing factors the rhizoid emerges at this point. Numerous environmental gradients, however, including light, gravity, temperature, and pH, may act as final determinants of the polar axis. The zygote settles onto a substrate , and a rhizoidal outgrowth develops from one side of the cell. Following nuclear division, a new cell wall separates cells that have different developmental fates: a hemispherical cell that will form the thallus , and a rhizoidal cell that will form the holdfast.

The process of polar axis fixation involves a current of calcium ions moving into the cell at the site of future rhizoid emergence and the accumulation of calcium channels in the membrane at this site. Actin filaments then accumulate, and Golgi-derived vesicles containing cell wall precursors migrate through the cytoplasm and release their contents at the site of rhizoid formation. All these events precede division of the zygote into two cells, so that it is the zygote itself that becomes polarized.

In angiosperms , the egg is already polarized at the time of fertilization. The nucleus and most of the cytoplasmic organelles are located near the apical end of the cell and a large vacuole occupies much of the basal (lower) half. Division of the zygote is transverse , separating a small cytoplasmically rich apical cell that forms all or most of the embryo from a large vacuolated basal cell that forms the extraembryonic suspensor.

It has been proposed that auxin establishes the polar axis in angiosperm embryos, as it does in Fucus zygotes. Movement of auxin through plant cells and tissues is polar from apex to base. This one-way transport is thought to depend on differential or polarized localization of membrane-associated auxin binding and transport proteins.

In the above examples, the result of cell division is the production of two cells that are visibly different and have different developmental fates. Such divisions are said to be asymmetric.

Asymmetric Cell Divisions

Asymmetric cell divisions are those in which there is unequal partitioning of cell components to the daughter cells. Examples are unequal distribution of cytoplasmic organelles, membrane components such as ion channels or pores, receptor molecules, or cell wall components. As a result of this differential inheritance of fate determinants from the mother cell, the daughter cells have different developmental fates, and this is the way that the term asymmetric cell division has been applied usually.

In the development of root epidermal cells of monocotyledons, cytoplasm accumulates at the end nearest the root tip, resulting in a polarized cell. This end is subsequently cut off by an asymmetric cell division, resulting in a small, cytoplasmically rich trichoblast ("hair precursor"), and a larger vacuolated epidermal cell. An outgrowth of the trichoblast develops as a root hair.

The formation of stomata, the pores that allow gas exchange between the atmosphere and internal tissues of leaves, involves both symmetric and asymmetric divisions. In most dicotyledons a developing epidermal cell divides asymmetrically to form a small triangular cell (when viewed from the surface). This cell, termed a meristemoid because it continues to divide after adjacent cells have ceased division, divides symmetrically to form two identical stomatal guard cells that form the pore, or in some species it may undergo several divisions before forming the guard cells.

Another important asymmetric division is the division of the microspore, separating a small, cytoplasmically rich generative cell that forms the male gametes from a larger vegetative cell. This is the first division in pollen development and separates two cells with different developmental fates. In mutants where this division is affected, either the division fails to occur or it is symmetric. In either case pollen development fails, indicating the importance of the asymmetric division to this process.

Positional Information in Cell Differentiation

The consequences of cell polarity and asymmetric divisions are to place sister cells of a mitotic division in different cellular environments, such as closer to or farther from the tip of the organ or to the inside or outside in a tissue. These cells, occupying different positions, may then be receptive to different external information, and this is the basis for the concept of positional information. Although the concept has a long history in developmental biology, it was Lewis Wolpert in 1971 who formalized it.

Positional information has been invoked to explain many developmental processes but there are relatively few in which it has been subjected to experimental analysis. One of the best examples is the development of root hairs in Arabidopsis. The root epidermis consists of files of root-hair-bearing trichoblasts alternating with files of hairless cells. Trichoblasts occupy predictable positions over the radial walls of underlying cortical cells. This suggests that the alternating pattern of trichoblast files is determined by the positions they occupy, and it has been proposed that the gaseous plant hormone ethylene is produced in the radial wall boundaries of cortical cells and activates root-hair formation. Mutants that vary in their response to ethylene confirm this suggestion, indicating that the molecular basis of positional information in this case had been identified.

see also Anatomy of Plants; Embryogenesis; Genetic Mechanisms and Development; Germination and Growth; Hormonal Control and Development; Meristems; Senescence; Tissues.

Ian Sussex

Nancy Kerk

Bibliography

Gallagher, Kimberly, and Laurie G. Smith. "Asymmetric Cell Division and Cell Fate in Plants." Current Opinion in Cell Biology 9 (1997): 842-48.

Jürgens, Gerd, Markus Grebe, and Thomas Steinmann. "Establishment of Cell Polarity in Plant Development." Current Opinion in Cell Biology 9 (1997): 849-52.

Lyndon, Robert F. Plant Development: The Cellular Basis. London: Unwin Hyman, 1990.

Scheres, Ben. "Cell Signalling in Root Development." Current Opinion in Genetics and Development 7 (1997): 501-06.

Wardlaw, Claude W. "A Commentary on Turing's Diffusion-Reaction Theory of Morphogenesis." New Phytologist 52 (1953): 40-47.

Wolpert, Lewis. "One Hundred Years of Positional Information." Trends in Genetics 12 (1996): 359-64.