Cell Rearrangements in Sequentially Segmenting Arthropods: The Tribolium Model
How comparable is this model from Drosophila to what is known in other arthropods? Tribolium is one of the few sequentially segmenting arthropods that has been analyzed with any molecular detail in regard to cell rearrangement. The first notable movements of cells in the Tribolium blastoderm are of a population of cells that condense in the posterior of the egg to form the germband and become distinct from more anterior blastoderm cells destined to form extraembryonic tissues (see blastoderm fate map in Benton, 2018). Thus, the embryonic cells have already migrated significantly from a relatively uniform blastoderm field prior to elongation of the germband per se. Subsequently, elongation occurs progressively, in the posterior region as new segments are specified. In addition to this apparent progressive elongation, live imaging of embryos shows periodic whole germband contractions, suggestive of myosin contractility. Overall the process of elongation in Tribolium is phenomenologically distinct from Drosophila in that it occurs in a changing cell field, the boundaries of which are changing as new segments form, and has dynamic regulatory inputs, as we describe in the following.
Live Imaging Shows Clear Convergent Extension in the Tribolium Germband
The dynamic behavior of cells during Tribolium embryo elongation has recently been analyzed using live imaging and fluorescent reporters. By tracing a subset of cell movements over one hour in the early germband (during the transition from pair- rule stripe 3 to pair-rule stripe 4), Sarrazin et al. (2012) provided evidence that cells in the early germband undergo medially directed movements that drive convergent extension: cells in the anterior of the germband move medially and anteriorly, cells in the posterior of the germband move medially and posteriorly as the germband narrows. Subsequently, Benton et al. (2013) tracked seven rows of cells during a slightly earlier stage, in what appear to be the anterior region of the lateral ectoderm (location in the embryo was not indicated but it appears to be the region that will express pair-rule stripes 1 and 2). They showed cells rearrange mediolaterally as the tissue lengthens during the hour of filming, providing clear evidence for convergence and extension. More recently, Benton (2018) also tracked cells in the posterior growth zone during abdominal segment formation. His rows of marked cells clearly mix and elongate during the 3 hours (25-28°C) of filming.
220.127.116.11 Tribolium Convergent Extension Does Not Appear to Arise from a Drosophila-Like Neighbor-Sliding Mechanism
Although these Tribolium studies show clear convergent extension behavior, what is occurring mechanistically and how comparable it is to Drosophila is not clear. One way to consider this is to compare marked cells in the Drosophila germband to those in the elongating Tribolium germband (Figure 3.8). Cell tracking in Drosophila clearly shows the orderly movement of cells (Irvine and Weischaus, 1994) by the coordinated junctional remodeling and basolateral interdigitation described earlier. Rows of marked cells extend in the AP direction as regularly spaced unmarked cells move past them. Rows remain roughly parallel as they move toward one another along the DV axis (Irvine and Weischaus, 1994) and the endpoint shows each of the marked cells separated by a single unmarked cell—the classic model of cell intercalation. By contrast, while rows of cells along the AP axis intermingle in Tribolium, they do not appear to do so based on the kind of orderly underlying mechanism documented in Drosophila. Some cells change neighbors during elongation, others do not. Overall, there appears to be differential movement both along the AP and DV axes (Figure 3.8B). In addition, in neither live imaging study were the rosettes of cells characteristic of junctional remodeling or basal protrusions reported, nor have polarized effectors of cell movement been documented in Tribolium (see later). Thus, while both species undergo convergent extension, the tracked movements of the cells show marked differences.