Cyclical Processes in Segmentation

The process of generating segments sequentially is by nature a cyclical process, with a sequence of events occurring repeatedly for every segment generated. The nature of this cyclical process has been studied in detail in some cases, whereas for others we have only a cursory understanding of what is involved.

The first system where cyclical segmentation was described, and the one for which we still have the largest body of data, is vertebrate somitogenesis (Pourquie, 2003). In this process, a traveling wave of gene expression moves over a field of undifferentiated mesodermal cells. At some point, the traveling wave is fixed in space, giving a repeating pattern of cell identities, which is translated into the reiterated pattern of mesodermal somites. This process is very similar to the process predicted by one of the earliest theoretical models for how repeated units can be patterned during development, the clock and wavefront model (Cooke and Zeeman, 1976). We now know that the traveling wave is maintained through entrainment of adjacent cells using Notch-Delta signaling, and a cell autonomous Hairy-based clock, and it is fixed in space through interactions with a Wnt-signaling gradient (Aulehla and Herrmann, 2004; Dubrulle and Pourquie, 2004).

Evidence of traveling waves involved in generating a segmental pattern also exists in several groups of arthropods, although the molecular mechanism behind them is probably very different, suggesting they have evolved convergently. In the centipede Strigamia, a traveling wave of expression of delta and several other segmental genes sweeps across the large posterior undifferentiated disk (Chipman and Akam, 2008). The nature of the original cycler and the mode of propagation of the wave remain unknown. Similar traveling waves have also been shown in spider development (Schoppmeier and Damen, 2005a). In the spider example there is also an involvement of the Notch pathway (Stollewerk et al., 2003; Schoppmeier and Damen, 2005b), but again, the exact details are unclear. A very different type of cycler and traveling wave has been reported from the flour beetle Tribolium. Here, the cycler is based on a negative feedback loop between three genes, which are orthologs of Drosophila pair-rule genes. The negative feedback generates a reiterated pattern, with each repeat generating a two-segment unit (Choe et al., 2006). In contrast, in the hemimetabolous insect Oncopeltus, there is no evidence of any type of traveling wave, and the nature of the repeating process, which generates single-segment units, is unknown (Auman et al., 2017; Auman and Chipman, 2018).

A cyclical signal moving across cells is not the only way to generate a repeated pattern in development. An alternative way to make a repeated pattern is to link patterning with the cell division cycle. This is indeed what happens in malacostracan crustaceans (Chapter 6) and in clitellate annelids (Chapter 7). In both these cases, a single cycle of cell division is linked to the generation of the precursors of a single segmental unit. A series of dedicated stem cells, known as teloblasts, divide asymmetrically, giving rise to one daughter cell that will serve as a segmental precursor cell, and one daughter cell that maintains stem properties. Essentially, the segmentation process is regulated by the same factors that regulate the cell cycle. It remains unclear at what level the ancestral segmentation gene regulatory network comes in to the process.

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