Maintaining bilateral symmetry and terminal development in early Drosophila embryogenesis

Abstract

Bilateral symmetry defines much of the animal kingdom and is crucial for numerous functions of bilaterian organisms. Genetic approaches have discovered highly conserved patterning networks that establish bilateral symmetry in early embryos (Genikhovich & Technau, 2017), but how this symmetry is maintained throughout subsequent morphogenetic events remains largely unknown (Grimes, 2019). Here I show that the terminal patterning system – which relies on Ras/ERK signaling through activation of the Torso receptor by its ligand Trunk (Smits & Shvartsman, 2020) – is critical for preserving bilateral symmetry during Drosophila body axis elongation, a process driven by cell rearrangements in the two identical lateral regions of the embryo and specified by the dorsal-ventral and anterior-posterior patterning systems (Kong et al., 2017). I demonstrate that fluctuating asymmetries in this rapid convergent-extension process are attenuated in normal embryos over time, possibly through noise-dissipating forces from the posterior midgut invagination and movement. However, when Torso signaling is attenuated via mutation of Trunk or RNAi directed against downstream Ras/ERK pathway components, body axis elongation results in a characteristic corkscrew phenotype (Perkins et al., 1992), which reflects dramatic reorganization of global tissue flow and is incompatible with viability. These results reveal a new function downstream of the Drosophila terminal patterning system in potentially active control of bilateral symmetry and should motivate systematic search for similar symmetry-preserving regulatory mechanisms in other bilaterians. Additionally, I present a framework for imaging the lineages of pole cell, the primordial germ cells of the embryo, and I show preliminary data on these lineage traces that depicts pole cell division patterns.