Modification of Spiralian Specification

Nemertean cleavage

In 1898, E. B. Wilson presented a famous lecture wherein he concluded that all spiralians—molluscs, flatworms, anelids, and nemerteans—shared a common evolutionary ancestry. The early development of these organisms were found to be remarkably similar, and cell lineage studies showed that the origins of the larval and adult ectoderm, mesoderm, and endoderm were homologous between these phyla (Costello and Hensly, 1976).

In annelids and molluscs, the first four cells, A, B, C, and D define the future axes of the larva and adult, giving rise to the left, ventral, right, and dorsal anterior structures, respectively. The posterior structures are generated from the D blastomere which also gives rise to the visceral mesoderm (and organizes early development, as mentioned in the text).

In nemerteans, each of the four blastomeres establishes a particular territory, but the cell fates of the four quadrants of nemertean cleavage are not homologous to those of the mollusc or annelid embryos. In nemerteans, the first two cleavage planes correspond to the bilateral and frontal planes. The first two divisions in molluscs and annelids are oblique to the dorsoventral axis. Furthermore, there is not a "D" lineage that generates the majority of posterior cells in the nemerteans. Figure 1 shows the lineage relationships between the first four blastomeres in two types of nemertean, the direct-developing Nemertopsis bivittata and the pilidium larva-producing Cerebratulus lacteus.

Figure 1
Figure 1   Relationship between cell division planes and the fates of the cell lineages in C. lacetus (upper) and N. bivittata (lower). The first two cleavages are interchangeable and converge at the same four-cell stage. (The small circles represent polar bodies). In Cerebratulus, the larva is divided into left and right dorsal (LD and RD) and left and right ventral (LV and RV) quadrants. In Nemertopsis, the same cells produce the left and right dorsal (LD and RD) and left and right lateral (LL and RL) quadrants. (After Martindale and Henry, 1995).

Martindale and Henry (1995) have looked at the ability of the nemertean cells to regulate. By deletion and cell lineage mapping with fluorescent dyes, they have found that the specification of the nemertean cells may be made in a unque manner, different from those of annelids and molluscs. The deficiencies of Nemertopsis embryos did not correspond to those predicted from the molluscan fate map. Rather, they seemed about 45 degrees out of register. These data have given rise to the model shown in Figure 2.

Figure 2
Figure 2   Proposed model of Martindale and Henry to explain discrepancies between molluscan and nemertean blastomere isolation experiments. The placement of the determinants is similar, but the relationship between the first two cleavage planes and the future dorsal-ventral axis has shifted 45 degrees.

The 4-cell stage of annelids and molluscs and the nemertea are shown, and the future dorsal-ventral axis is shown in relation to these cells. The A and C blastomeres of molluscs produce eyes (whose postulated determinant is indicated by the small letter e). The distribution of this determinant is such that in the next (dextrotropic) spiral cleavage, the determinant will be apportioned to the first quartet micromeres. The molluscan D blastomere (shaded blue here) forms the dorsal and posterior regions of the larvae. On the right, the nemertean embryo can be seen. The placement of the eye determinant and the molluscan D-lineage determinants (blue) are in similar places, but the relationship of the cleavage planes to the dorsal-ventral axis has shifted 45 degrees. This places the eye determinants in different blastomeres and causes some of the eye determinants to be in the same cell (RD) that gives rise to some of the posterior cells. The D-blastomere determinants are now in two cells instead of just one.

It seems that during evolution, some things remain constant and some things change. In some ways, these experiments show how remarkably similar the nemerteans are to the molluscs. Their determinants appear to be arranged very similarly within the cytoplasm of the fertilized egg. However, the difference in the mitotic orientation with respect the the future dorsal-ventral axis apportions them into different cells. Such changes in the placement of cell determinants should be expected, especially given the different life history strategies of spiralians and what larval organs they must make.

Leech cleavage

In leech (annelid) embryos, cell fates are also highly stereotypes. One of the first events is the separation of the ectodermal lineage from the mesodermal lineage. This occurs when the D' blastomere makes an oblique division at the fourth cleavage (Figure 3).

Figure 3
Figure 3   Summary of the development of the leech Helobdella robusta. (A) Yolk-deficient teloplasm forms at both the animal and vegetal caps of the zygote. (B) At first cleavage, the larger, CD cell, inherits both caps of teloplasm. (C) In the next cleavage, the D blastomere retains both teloplasmic caps, and the vegetal teloplasm begins migrating towards the animal teloplasm. The two plasms will merge at the animal pole. (D) The 8-cell embryo. Third cleavage produces a set of very small micromeres and a set of large vegetal macromeres. The D' cell contains all the teloplasm near its animal cap. (E) The 12-cell embryo. D' divides into DNOPQ (which forms near the animal pole) and DM (which forms more vegetally). Each of these cells contains some teloplasm. (F) DNOPQ produces four bilateral pairs of ectodermal teloblasts (N, O/P, O/P, and Q) and 13 micromeres. DM produces one pair of mesodermal teloblasts (the M mesoteloblasts) and two micromeres. (G) The teloblasts produce bandlets of cells. Left, the mesodermal teloblast and the bandlet of cells derived from DM. Right, the four ectodermal teloblasts and the bandlets derived from DNOPQ. Lower case letters indicate bandlet identities. The four ectodermal bandlets form a sheet that covers the mesodermal bandlet. The five bandlets are called the "germinal band." The right and left germinal bands are mirror-images of each other (only one shown here), joined at the future ventral midline. (After Nelson and Weisblat, 1992).

The teloplasms are extremely important for the ectoderm/mesoderm distinction. When animal teloplasm was removed from the animal pole of the zygote, the ectodermal precursor (DNOPQ) is converted to a mesodermal fate. This conversion can be prevented if the extruded animal teloplasm is replaced by vegetal teloplasm. Mesodermal cell fate was not changed when the teloplasm was removed (Nelson and Weisblat, 1991). Mesoderm appears to be the ground state of the cell, and the ectodermal determinants alter its identity. These ectodermal determinants are thought to be localized in the cortex of the animal pole of the egg. However, they need to interact with factors in the teloplasm in order to transform the fate of the DNOPQ cell from mesoderm to ectoderm. This was shown by reorienting first cell division by pressure such that the animal and vegetal hemispheres were isolated from each other. The epidermal fate was found to segregate with the animal hemisphere, the mesodermal fate with the vegetal hemisphere. The DNOPQ cell, but not the DM cell, is capable of forming ectoderm if it has teloplasm. Thus, both the ectodermal determinants (cortical and animal) and the teloplasm (of the deep cytoplasm) are critical for the production of the ectodermal cells (Figure 4).

Figure 4
Figure 4   Model for leech ectoderm determination. The teloplasm is stippled and the hatched lines in the animal cortex represent the ectodermal determinant. (A) Normal development, wherein the D blastomere gets both teloplasm and part of the cortical ectodermal determinants. This leads to the production of a cell that can make ectoderm (E; the DNOPQ cell) and one that can make only mesoderm (M; the DM cell). (B) If the first cleavage is oblique such that both AB and CD cells incoporate teloplasm and have the ectodermal determinants, two sets of DM and DNOPQ cells form. (C) If the cleavage plane is made such that the vegetal pole is separated from the animal pole, the animal pole makes the ectoderm, the vegetal cell makes the mesoderm.

Thus, the leech is also an exception to the general spiralian rule that the morphogenetic determinants are strictly D-blastomeric property. Although the developmental "ends" are the same--assignment of mesodermal and ectodermal fates to the animal and vegetal progeny of the D blastomere--there are multiple means to achieve this end.

Literature Cited

Costello, D. P. and Henley, C. 1976). Spiralian development: A perspective. Amer. Zool. 16: 277-291.

Martindale, M. Q. and Henry, J. Q. 1995. Modifications of cell fate specification in equal-cleaving nemertean embryos: Alternate patterns of spiralian development. Development 121: 3175-3185.

Nelson, B. H. and Weisblat, D. A. 1991. Conversion of ectoderm to mesoderm by cytoplasmic extrusion in leech embryos. Science 253: 435-438.

Nelson, B. H. and Weisblat, D. A. 1992. Cytoplasmic and cortical determinants interact to specify ectoderm and mesoderm in the leech embryo. Development 115: 103-115.

Wilson, E. B. 1898. Cell-lineage and ancestral remiscence. In Biological Lectures M. B. L., Woods Hole. Ginn and Co., Boston. pp. 21-42.

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