The Role of Cell Division

Many species, whether they develop from a sequentially segmenting embryo or larva, appear to add their new segments from a region at the posterior of the embryo/larva. Consequently, both the addition of new segments and the driving force for elongation were originally hypothesized to result from cell division in this posterior domain (Anderson, 1973; Sander, 1975). In its simplest form, a posterior “growth zone” would supply both naive tissue for segment patterning at its anterior border and all the additional tissue required for elongation (Figure 3.1). As our understanding of the cellular mechanisms that drive elongation have grown, we now understand that segment addition can be accomplished by posteriorly localized stem cells (e.g., malacostra- cans; reviewed in Dohle and Scholtz, 1997; Scholtz and Wolff, 2013; and Chapter 6) or migration of cells (Benton, 2018), or by having a population of cells that divide until they exit the posterior, presumably held in a multipotent state by a posterior signal (Shinmyo et al„ 2005; McGregor et ah, 2008, 2009; Chesebro et ah, 2013; Constantinou et ah, 2016; Williams and Nagy, 2017). In addition, elongation in many species is driven by cell division and rearrangements outside of the posteriormost region of the embryo or larva (see following discussion). This diversity of mechanism led to the suggestion to replace the classical term “growth zone” with the term “segment addition zone” (Janssen et ah, 2010). As both terms imply posterior growth and both terms are essentially agnostic to mechanism, we have argued for retaining “growth zone” as a generally understood term for the area from which the germband grows—albeit using a diversity of cellular mechanisms (Auman et ah, 2017).

Case Studies Support a New Model for the Role of Cell Division in the Posterior

We describe three case studies examining cell division in the posterior: a non- malacostracan crustacean and two different insect species. These cases (as well as other published literature reviewed) illustrate the role of cell division in our

Various cell behaviors that could account for elongation during segmentation in sequentially segmenting arthropods

FIGURE 3.1 Various cell behaviors that could account for elongation during segmentation in sequentially segmenting arthropods. Classical models of a growth zone (A and B) have assumed high rates of cell division in the posterior. Cell division could be limited to stem cells (C), although that has been found in only one crustacean clade (Malacostraca). When actually measured, mitoses appear much more widespread within the embryo (D), usually without a posterior bias. Other known methods of elongation include cell migration (E) and intercalation (F). (Mitotic cells, red; Engrailed/Invected expressing cells, green; see text for references).

proposed model and suggest some common principles of elongation. First, cell division promoting elongation is distributed throughout the embryo or larvae, and is not a consequence of a continually or even highly proliferative posterior growth zone. Second, in most species, the growth zone shrinks over the course of segmentation, thus does in fact contribute to elongation of the embryo. However, its depletion is not sufficient to account for all the tissue of the newly added segments. Proliferation in the posterior growth zone is required for elongation but each cell in the growth zone need only divide a few times to supplement the contributions of growth from other regions of the embryo/larva. Third, the rate of cell division can vary over the course of elongation and cell cycle duration can be regulated, at least at times, by controlling the duration of cell cycle. Fourth, the region traditionally called the “posterior growth zone” is subdivided into a posterior domain of multipotent cells that divide infrequently, and an anterior domain of cells initiating segmental specification that rarely divide. All of these features have not yet been systematically analyzed in each case study, but in total provide a framework for future interspecies comparisons.

 
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