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Segmentation in annelids: Cellular and molecular basis for metameric body plan


Segmentation in annelids: Cellular and molecular basis for metameric body plan



Zoological Science 18(3): 285-298



ISSN/ISBN: 0289-0003

DOI: 10.2108/zsj.18.285

Annelids are segmented animals that display a high degree of metamerism in their body plan. This review describes the segmentation of clitellate annelids (i.e., oligochaetes and leeches) and polychaetes with special reference to cellular and molecular mechanisms elaborating the metameric body plan. In clitellate embryos, segments arise from five bilateral pairs of longitudinal coherent columns (bandlets) of primary blast cells that are generated by five bilateral pairs of embryonic stem cells called teloblasts (M, N, O, P and Q). Recent cell-ablation experiments have suggested that ectodermal segmentation in clitellates consists of two stages, autonomous morphogenesis of each bandlet leading to generation of distinct cell clumps (i.e., segmental elements; SEs) and the ensuing mesoderm-dependent alignment of separated SEs. In the N and Q lineages, SEs are each comprised of clones of two consecutive primary blast cells. In contrast, in the O and P lineages, individual blast cell clones are distributed across SE boundaries; each SE is a mixture of a part of a more-anterior clone and a part of the next more-posterior clone. In contrast, the metameric segmentation in the mesoderm (M lineage) is a one-step process in that it arises from an initially simple organization (i.e., a linear series) of primary blast cells, which individually serve as a founder cell of each segment; the boundary between mesodermal segments is determined autonomously. Cell-autonomous properties of primary blast cells have also been suggested in two fundamental aspects of segmentation, viz., specification of segment polarity and determination of segmental identities. Recent cell-ablation and -transplantation studies have suggested that segmental identities in primary blast cells derived from M teloblasts are determined according to the genealogical position in the M lineage and that the M teloblast possesses a developmental program through which the sequence of blast cell identities is determined. It is unlikely that either a segment polarity gene engrailed or Hoxgenes are involved in specifying polarity or identities of segments of clitellates, since these genes (in leeches) are reportedly expressed long after the establishment of these segmental properties. As in clitellates, segments in polychaetes arise from descendants of teloblasts located in a posterior growth zone, but it is only during trochophore larval stages that overt segmental organization becomes recognizable. At present, it is not known how the posterior growth zone generates trunk segments either during larval stages or after metamorphosis. However, the recent finding that Hox genes are expressed in the growth zone (probably in teloblasts) suggests that segmentation mechanisms in polychaetes are distinct from those in clitellates.

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