The Leech PGZ Provides a Highly Simplified and Experimentally Accessible Example of Axial Growth and Patterning

During segmentation, each teloblast undergoes a series of several dozen highly unequal stem cell divisions (Figure 7.3). The smaller daughter cell at each division is called a blast cell and is designated with the lowercase letter corresponding to the teloblast of origin. The blast cells exhibit significantly prolonged cell cycle durations (12-44 hours to their first mitosis, depending on the lineage), while the teloblasts divide with cell cycle times of 75 to 90 minutes (depending on the temperature and the species). Moreover, in each lineage, each newly born blast cell maintains contact with the blast cell formed in the previous division. Thus, the progeny of each telo- blast arise in a remarkably well-ordered column of cells (called a bandlet), within which the blast cells are strictly arranged according to birth order (Figure 7.3). The five bandlets on each side of the embryo coalesce ipsilaterally, forming an array of parallel bandlets called the germinal band (Figure 7.3). The germinal bands and the region between them are covered by a micromere-derived squamous epithelium.

As teloblast divisions add cells to the posterior ends of the germinal bands, the germinal bands lengthen and move over the surface of the embryo, eventually coalescing to form a bilaterally symmetric sheet of cells called the germinal plate (Figures 7.3 and 7.4). Concomitantly, the micromere-derived epithelium spreads to cover the surface of the embryo, providing it with a temporary protective covering. The germinal plate forms in anteroposterior progression (i.e., starting with the cells distal to the teloblasts) along the ventral midline of the embryo (Figures 7.3 and 7.4).

In the Helobdella embryo, the germinal plate initially wraps most of the way around the spherical, yolk-rich embryo, so that its anterior and posterior end are close to one another. During subsequent stages of development, cell proliferation and differentiation of segmental tissues within the germinal plate cause it to gradually expand dorsolaterally and straighten out, eventually meeting along the dorsal midline of the embryo and completing the formation of the tubular leech body plan. During this process, the yolky core elongates and is converted to midgut.

The bandlets within the left and right germinal bands are arrayed in a stereotyped manner—the four ectodermal bandlets lie superficial to the mesodermal bandlet, and in alphabetic order (now designated n, o, p, and q) so that the n bandlets are at the leading edge of the germinal bands, and come into direct apposition along the ventral midline as the germinal bands coalesce to form the germinal plate (Figures 7.3 and 7.4). As cells proliferate and differentiate during later stages of development, the lateral edges of the germinal plate move dorsally around the yolk cells, eventually zippering together along the dorsal midline to form the tubular body of the adult leech. This broad understanding of the development of glossiphoniid leeches was provided by C.O. Whitman in the 19th century (Whitman 1878). Roughly one century later, the development and application of cell lineage tracing by microinjection of precursor cells with marker enzymes or fluorophores (Weisblat et al. 1978, 1980; Gimlich and Braun 1985) opened the door to a more detailed understanding of leech development in general and segmentation in particular.

Injecting individual teloblasts with lineage tracers revealed that segmental mesoderm and ectoderm arise as the composite of five segmentally repeating, bilaterally symmetric patterns of cells. As will be described in Section 7.8, these segmentally iterated patterns are not simply blast cell clones, and are therefore designated as M, N, О, P, and Q “kinship groups,” respectively, defined as all the cells within one segment that arise from the corresponding teloblast (the relationship between the ambiguously named О/P teloblasts and the distinct О and P kinship groups will be detailed in Section 7.9).

Axial growth from the posterior end of the embryo, accompanied by patterning in an anteroposterior progression are common traits of embryos in all three of the bilaterian superphyla. Thus, it seems likely that this feature may have been present in the bilaterian ancestor. In most such embryos, however, as cells exit the posterior zone to generate segments or other axially patterned tissues, they are replaced by a poorly characterized and perhaps variable mixture of cell proliferation, including stem cell processes, and cell movements, i.e., influx of cells from other parts of the embryos (see Chapter 2). Uncertainty as to whether the posterior zone is replenished by growth (cell division) or cell movements has led to this region being called a segment addition zone (Janssen et al. 2010).

By contrast, in leeches and certain crustacean embryos (see Chapter 6), the more precise term of PGZ is appropriate because the segmental founder cells arise entirely via stem cell divisions of a small number of relatively large and individually identifiable cells. The presence of teloblastic PGZs in leeches and crustaceans was at one point taken as evidence for the Articulata hypothesis, i.e., a shared origin of their segmentation processes in a common ancestor of annelids and arthropods (Giribet 2003). In light of current molecular phytogenies, and with a better understanding of the limited similarities and significant differences between leeches and crustaceans PGZs, we now view these similarities as further evidence for evolutionary plasticity of development.

 
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