Article,

Dynamic patterning by the Drosophila pair-rule network reconciles long-germ and short-germ segmentation

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PLOS Biology, 15 (9): 1-38 (September 2017)
DOI: 10.1371/journal.pbio.2002439

Abstract

Author summary Segmentation in insects involves the division of the body into several repetitive units. In Drosophila embryos, all segments are patterned rapidly and simultaneously during early development, in a process known as “long-germ” embryogenesis. In contrast, many insect embryos retain an ancestral or “short-germ” mode of development, in which segments are patterned sequentially, from head to tail, over a period of time. In both types of embryo, the patterning of segment boundaries is regulated by a network of so-called “pair-rule” genes. These networks are thought to be quite divergent due to the different expression patterns observed for the pair-rule genes in each case: regularly spaced arrays of transient stripes in Drosophila, and dynamic expression within a posterior “segment addition zone” in short-germ insects. However, even in Drosophila, a clear understanding of pair-rule patterning has been lacking. Here, I make a computational model of the Drosophila pair-rule network and use simulations to explore how segmentation works. Surprisingly, I find that Drosophila segment patterning relies on pair-rule gene expression moving across cells over time. This conclusion differs from older models of pair-rule patterning but is consistent with the subtly dynamic nature of pair-rule stripes in real embryos, previously described in quantitative studies. I conclude that long-germ and short-germ segmentation involve similar expression dynamics at the level of individual cells, even though they look very different at the level of whole tissues. This suggests that the gene networks involved may be much more conserved than previously thought.

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