HOME :: CHAPTER 2 :: SLIME MOLD LIFE CYCLE :: THE EVOLUTION OF DEVELOPMENTAL PATTERNS IN UNICELLULAR PROTISTS

The Evolution of Developmental Patterns in Unicellular Protists

Every living organism develops. Development can be seen even among the unicellular organisms. Moreover, by studying the development of unicellular protists, we can see the simplest forms of cell differentiation and sexual reproduction.

Control of developmental morphogenesis: The role of the nucleus

A century ago, it had not yet been proved that the nucleus of the cell contained hereditary or developmental information. Some of the best evidence for this theory came from studies in which unicellular organisms were fragmented into nucleate and anucleate pieces (reviewed in Wilson 1896). When various protists were cut into fragments, nearly all the pieces died. However, the fragments containing nuclei were able to live and to regenerate entire complex cellular structures.

Nuclear control of cell morphogenesis and the interaction of nucleus and cytoplasm are beautifully demonstrated in studies of the protist Acetabularia. This enormous single cell (2–4 cm long) consists of three parts: a cap, a stalk, and a rhizoid (Figure 1A; Mandoli 1998). The rhizoid is located at the base of the cell and holds it to the substrate. The single nucleus of the cell resides within the rhizoid. The size of Acetabularia and the location of its nucleus allow investigators to remove the nucleus from one cell and replace it with a nucleus from another cell. In the 1930s, J. Hämmerling took advantage of these unique features and exchanged nuclei between two morphologically distinct species, A. mediterranea* and A. crenulata. As Figure 1A shows, these two species have very different cap structures. Hämmerling (1934) found that when he transferred the nucleus from one species into the stalk of another species, the newly formed cap eventually assumed the form associated with the donor nucleus (Figure 1B). Thus, the nucleus was seen to control Acetabularia development.

Figure 1 (A) Acetabularia crenulata (left) and A. mediterranea (right). Each individual is a single cell. The rhizoid contains the nucleus. (B) Effect of exchanging nuclei between two species of Acetabularia. Nuclei were transplanted into enucleated rhizoid fragments. A. crenulata structures are darker, A. mediterranea structures lighter green. (Photographs courtesy of S. Berger.) (Click image to enlarge.)

The formation of a cap is a complex morphogenic event involving the synthesis of numerous proteins, which must be accumulated in a certain portion of the cell and then assembled into complex, species-specific structures. The transplanted nucleus does indeed direct the synthesis of its species-specific cap, but it takes several weeks to do so. Moreover, if the nucleus is removed from an Acetabularia cell early in its development, before it first forms a cap, a normal cap is formed weeks later, even though the organism will eventually die. These studies suggest that (1) the nucleus contains information specifying the type of cap to be produced (i.e., it contains the genetic information that specifies the proteins required for the production of a certain type of cap), and (2) material containing this information enters the cytoplasm long before cap production occurs. This information in the cytoplasm is not used for several weeks.

One current hypothesis proposed to explain these observations is that the nucleus synthesizes a stable mRNA that lies dormant in the cytoplasm until the time of cap formation (Dumais et al. 2000). This hypothesis is supported by an observation that Hämmerling published in 1934. Hämmerling fractionated young Acetabularia into several parts (Figure 2). The portion with the nucleus eventually formed a new cap, as expected; so did the apical tip of the stalk. However, the intermediate portion of the stalk did not form a cap. Thus, Hämmerling postulated (nearly 30 years before the existence of mRNA was known) that the instructions for cap formation originated in the nucleus and were somehow stored in a dormant form near the tip of the stalk. Many years later, researchers established that nucleus-derived mRNA does accumulate in the tip of the stalk, and that the destruction of this mRNA or the inhibition of protein synthesis in this region prevents cap formation (Kloppstech and Schweiger 1975; Garcia and Dazy 1986; Serikawa et al. 2001).

Figure 2 Regenerative ability of different fragments of A. mediterranea. (Click image to enlarge.)

It is clear from the preceding discussion that nuclear transcription plays an important role in the formation of the Acetabularia cap. But note that the cytoplasm also plays an essential role in cap formation. The mRNAs are not translated for weeks, even though they are present in the cytoplasm. Something in the cytoplasm controls when the message is utilized. Hence, the expression of the cap is controlled not only by nuclear transcription, but also by the translation of the cytoplasmic RNA. In this unicellular organism, “development” is controlled at both the transcriptional and translational levels.

Unicellular protists and the origins of sexual reproduction

Sexual reproduction is another invention of the protists that has had a profound effect on more complex organisms. It should be noted that sex and reproduction are two distinct and separable processes. Reproduction involves the creation of new individuals. Sex involves the combining of genes from two different individuals into new arrangements. Reproduction in the absence of sex is characteristic of organisms that reproduce by fission (i.e., splitting into two); there is no sorting of genes when an amoeba divides or when a hydra buds off cells to form a new colony.

Sex without reproduction is also common among unicellular organisms. Bacteria are able to transmit genes from one individual to another by means of sex pili. This transmission is separate from reproduction. Protists are also able to reassort genes without reproduction. Paramecia, for instance, reproduce by fission, but sex is accomplished by conjugation. When two paramecia join together, they link their oral apparatuses and form a cytoplasmic connection through which they can exchange genetic material (Figure 3). The macronucleus of each individual (which controls the metabolism of the organism) degenerates, while each micronucleus undergoes meiosis to produce eight haploid micronuclei, of which all but one degenerate. The remaining micronucleus divides once more to form a stationary micronucleus and a migratory micronucleus. Each migratory micronucleus crosses the cytoplasmic bridge and fuses with (“fertilizes”) the partner’s stationary micronucleus, thereby creating a new diploid nucleus in each cell. This diploid nucleus then divides mitotically to give rise to a new micronucleus and a new macronucleus as the two partners disengage. Therefore, no reproduction has occurred, only sex.

Figure 3 Conjugation across a cytoplasmic bridge in paramecia. Two paramecia can exchange genetic material, each ending up with genes that differ from those with which they started. (After Strickberger 1985.) (Click image to enlarge.)

The union of these two distinct processes, sex and reproduction, into sexual reproduction is seen in other unicellular eukaryotes. Figure 4 shows the life cycle of Chlamydomonas. This organism is usually haploid, having just one copy of each chromosome (like a mammalian gamete). The individuals of each species, however, are divided into two mating types: plus and minus. When a plus and a minus meet, they join their cytoplasms, and their nuclei fuse to form a diploid zygote. This zygote is the only diploid cell in the life cycle, and it eventually undergoes meiosis to form four new Chlamydomonas cells. This is true sexual reproduction, for chromosomes are reassorted during the meiotic divisions and more individuals are formed. Note that in this protist type of sexual reproduction, the gametes are morphologically identical; the distinction between sperm and egg has not yet been made.

Figure 4 Sexual reproduction in Chlamydomonas. Two mating types, both haploid, can reproduce asexually when separate. Under certain conditions, the two mating types can unite to produce a diploid cell that can undergo meiosis to form four new haploid organisms. (After Strickberger 1985.) (Click image to enlarge.)

In the evolution of sexual reproduction, two important advances had to be achieved. The first was the mechanism of meiosis (Figure 5), whereby the diploid complement of chromosomes is reduced to the haploid state (discussed in detail in Chapter 19). The second was a mechanism whereby the two different mating types could recognize each other. In Chlamydomonas, recognition occurs first on the flagellar membranes (Figure 6; Bergman et al. 1975; Wilson et al. 1997; Pan and Snell 2000). The flagella of two individuals twist around each other, enabling specific regions of the cell membranes to come together. These specialized regions contain mating type-specific components that enable the cytoplasms to fuse. Following flagellar agglutination, the plus individual initiates fusion by extending a fertilization tube. This tube contacts and fuses with a specific site on the minus individual. Interestingly, the mechanism used to extend this tube—the polymerization of the protein actin to form microfilaments—is also used to extend the processes of sea urchin eggs and sperm. In Chapter 7, we will see that the recognition and fusion of sperm and egg occur in an amazingly similar manner.

Figure 5 Summary of meiosis. The DNA and its associated proteins replicate during interphase. During prophase, the nuclear envelope breaks down and homologous chromosomes (each chromosome is double, with the chromatids joined at the kinetochore) align in pairs. Chromosomal rearrangements between the four homologous chromatids can occur at this time. After the first metaphase, the two original homologous chromosomes are segregated into different cells. During the second meiotic division, the kinetochore splits and the sister chromatids separate, leaving each new cell with one copy of each chromosome. (Click image to enlarge.)

Figure 6 Two-step recognition in mating Chlamydomonas. (A) Scanning electron micrograph (7000×) of mating pair. The interacting flagella twist around each other, adhering at the tips (arrows). (B) Transmission electron micrograph (20,000×) of a cytoplasmic bridge connecting the two organisms. The actin microfilaments extend from the donor (lower) cell to the recipient (upper) cell. (From Goodenough and Weiss 1975 and Bergman et al. 1975; photographs courtesy of U. Goodenough.) (Click image to enlarge.)

Unicellular eukaryotes appear to possess the basic elements of the developmental processes that characterize more complex organisms: protein synthesis is controlled such that certain proteins are made only at certain times and in certain places; the structures of individual genes and chromosomes are as they will be throughout eukaryotic evolution; mitosis and meiosis have been perfected; and sexual reproduction exists, involving cooperation between individual cells. Such intercellular cooperation becomes even more important with the evolution of multicellular organisms.

*After a recent formal name change, this species is now called Acetabularia acetabulum. For the sake of simplicity, however, we will use Hämmerling’s designations here.

Literature Cited

Bergman, K., U. W. Goodenough, D. A. Goodenough, J. Jawitz and H. Martin. 1975. Gametic differentiation in Chlamydomonas reinhardtii. II. Flagellar membranes and the agglutination reaction. J. Cell Biol. 67: 606–622.

Dumais, J., K. Serikawa and D. F. Mandoli. 2000. Acetabularia: A unicellular model for understanding subcellular localization and morphogenesis during development. J. Plant Growth Reg. 19: 253–264.

Garcia, E. and A.-C. Dazy. 1986. Spatial distribution of poly(A)+ RNA and protein synthesis in Acetabularia mediterranea. Biol. Cell 58: 23–29.

Hämmerling, J. 1934. Über formbildended Substanzen bei Acetabularia mediterranea, ihre räumliche und zeitliche Verteilung und ihre Herkunft. Wilhelm Roux Arch. Entwicklungsmech. Org. 131: 1–82.

Kloppstech, K. and H. G. Schweiger. 1975. Polyadenylated RNA from Acetabularia. Differentiation 4: 115–123.

Mandoli, D. F. 1998. What ever happened to Acetabularia? Bringing a once-classic model system into the age of molecular genetics. Int. Rev. Cytol. 182: 1–67.

Pan, J. and W. J. Snell. 2000. Signal transduction during fertilization in the unicellular green alga Chlamydomonas. Curr. Opin. Microbiol. 3: 596–602.

Serikawa, K. A., D. M. Porterfield, and D. F. Mandoli. 2001. Asymmetric subcellular mRNA distribution correlates with carbonic anhydrase activity in Acetabularia acetabulum. Plant Physiol. 125: 900–911.

Wilson, E. B. 1896. The Cell in Development and Inheritance. Macmillan, New York.

Wilson, N. F., M. J. Foglesong and W. J. Snell. 1997. The Chlamydomonas mating type plus fertilization tubule, a prototypic cell fusion organelle: Isolation, characterization, and in vitro adhesion to mating type minus gametes. J. Cell Biol. 137: 1537–1553.

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