Evidence for the temporal regulation of insect segmentation by a conserved sequence of transcription factors

Abstract

Long-germ insects, such as the fruit fly Drosophila melanogaster, pattern their segments simultaneously, whereas short-germ insects, such as the beetle Tribolium castaneum, pattern their segments sequentially, from anterior to posterior. Although the two modes of segmentation at first appear quite distinct, much of this difference might simply reflect developmental heterochrony. We now show here that, in both Drosophila and Tribolium, segment patterning occurs within a common framework of sequential Caudal, Dichaete and Odd-paired expression. In Drosophila, these transcription factors are expressed like simple timers within the blastoderm, whereas in Tribolium they form wavefronts that sweep from anterior to posterior across the germband. In Drosophila, all three are known to regulate pair-rule gene expression and influence the temporal progression of segmentation. We propose that these regulatory roles are conserved in short-germ embryos, and that therefore the changing expression profiles of these genes across insects provide a mechanistic explanation for observed differences in the timing of segmentation. In support of this hypothesis, we demonstrate that Odd-paired is essential for segmentation in Tribolium, contrary to previous reports.

A sense of place, many times over ‐ pattern formation and evolution of repetitive morphological structures

“…Unlike in Drosophila , where Pair‐rule genes are concomitantly expressed in a striped pattern demarcating the future segments, dynamic waves of cyclic Pair‐rule gene expression propagate along the Tribolium growth zone, to sequentially segment the emerging primary body axis. Additionally, Caudal , Dichaete and Odd‐paired expression in Tribolium form spatiotemporally dynamic wavefronts that travel along the anterior‐posterior axis of the elongating embryo, while in Drosophila their sequential activation acts as a timer of Pair‐rule gene expression . Hence, although displaying drastically different growth modes for axis elongation, in both long‐germ and short‐germ insect segmentation similar sets of orthologous genes are essential in anterior‐posterior pattern formation.…”

“…Hence, although displaying drastically different growth modes for axis elongation, in both long‐germ and short‐germ insect segmentation similar sets of orthologous genes are essential in anterior‐posterior pattern formation. The underlying genetic circuitries thus seem to contain an ability to compute and execute analogous patterning functions, both within static embryonic fields as well as along progressively elongating domains . Disparities in their regulatory architectures, though, between long‐germ and short‐germ insects, emphasize the importance of properly integrating temporally dynamic gene expression programs with positional information in directionally growing domains .…”

“…Additionally, Caudal, Dichaete and Odd-paired expression in Tribolium form spatiotemporally dynamic wavefronts that travel along the anterior-posterior axis of the elongating embryo, while in Drosophila their sequential activation acts as a timer of Pair-rule gene expression. 47 Hence, although displaying drastically different growth modes for axis elongation, in both long-germ and short-germ insect segmentation similar sets of orthologous genes are essential in anteriorposterior pattern formation. The underlying genetic circuitries thus seem to contain an ability to compute and execute analogous patterning functions, both within static embryonic fields as well as along progressively elongating domains.…”

“…[47][48][49] Disparities in their regulatory architectures, though, between long-germ and short-germ insects, emphasize the importance of properly integrating temporally dynamic gene expression programs with positional information in directionally growing domains. 47,49,50 The fact that short-germ band insects do not seem to exploit their mode of axis elongation to increase overall segment number, like for example in the vertebral column of snakes (see below), may hint at an underlying developmental constraint, originating from molecular crosstalk between the two systems in insects. 42,51 Intriguingly, though, primary body axis patterning in other arthropod clades such as the Myriapoda clearly is more variable, with overall segment numbers in for example, geophilomorph centipedes ranging from 27 to 191.…”

Fog signaling has diverse roles in epithelial morphogenesis in insects

“…To test whether Fog signaling does have a more widely conserved role in early development, we have analyzed Fog pathway components in the beetle Tribolium castaneum. In contrast to Drosophila and other dipteran species like Chironomus, many features of Tribolium embryogenesis are more typical of insects in general, including the mechanism and timing of blastoderm cellularisation (van der Zee et al, 2015), the mode of germ cell formation (Schroder, 2006), germband formation (Benton, 2018), extraembryonic tissue development (Hilbrant et al, 2016;Horn and Panfilio, 2016;van der Zee et al, 2005) and segmentation (Clark and Peel, 2018;Sommer and Tautz, 1993). Therefore, analyzing Fog signaling in Tribolium will reveal the role of the pathway within a developmental context that is more representative of insects.…”