Role of Pair-Rule Genes in Elongation in Tribolium
Despite distinct cell movements, Tribolium shares w'ith Drosophila some regulatory control of elongation: in both species, elongation depends on pair-rule gene function. During Tribolium elongation, pair-rule expression is dynamic in the posterior, with cells undergoing oscillatory expression of pair-rule genes while they undergo the movements that constitute convergence and extension (Figure 3.3B; Choe et al., 2006; Sarrazin et al., 2012; El-Sherif et al., 2012). Cellular oscillations of pair-rule gene expression are regulated by a posterior gradient of Caudal protein (El-Sherif et al., 2014) and produce a wave of expression that travels from the posterior anteriorly during elongation. When it reaches the anterior, the wave stabilizes, then splits into two stripes. The result is the progressive formation of stable, segmentally iterated stripes, first, of pair-rule genes, subsequently of segment polarity genes (e.g., engrailed; Sarrazin et al., 2012; El-Sherif et al., 2012). Loss of caudal function results in severely truncated embryos that fail to undergo the wild-type cell movements that restructure the blastoderm into the initial germband (Copf et al., 2004; Schoppmeier et al., 2009; Benton et al., 2013). Parental and embryonic RNAi knockdowns of the Tribolium pair-rule genes eve, odd, and runt also result in truncated embryos: arrest occurs just after the initial condensation of the blastoderm cells into the germband (Choe et al., 2006; Nakamoto et al., 2015). Moreover, we have demonstrated that clones marked in the blastoderm do not elongate in eve knockdowns in Tribolium, consistent with a role for eve in regulation of elongation (Figure 3.4; Nakamoto et al., 2015). Thus, both flies and beetles show a similar failure to elongate in pair-rule gene mutants. However, the timing of the onset of cell movement relative to the expression of pair-rule genes differs dramatically between the two species. While the Drosophila pair-rule genes undergo dynamic expression patterns, those dynamics have stabilized in all but the most posterior segments prior to the onset of germband elongation (Kuhn et al., 2000; Clark, 2017; Clark and Peel, 2018). In Tribolium, dynamic pair-rule expression patterns accompany elongation. Clark and Peel (2018) argue that the upstream regulation of segment patterning is essentially the same in both species but varies mostly in temporal readout in long germband versus short germband insects. Whether the same can be hypothesized about the regulation of elongation per se remains unknown.