TY - JOUR
T1 - Maintaining symmetry during body axis elongation
AU - Smits, Celia M.
AU - Dutta, Sayantan
AU - Jain-Sharma, Vishank
AU - Streichan, Sebastian J.
AU - Shvartsman, Stanislav Y.
N1 - Funding Information:
Research reported in this publication was supported by NIGMS of the NIH under grant number T32GM007388 (to Princeton Molecular Biology) and NIH Research Grant RO1GM134204 (to S.Y.S.). We would like to thank Gary Laevsky and the Confocal Imaging Facility, a Nikon Center of Excellence, in the Department of Molecular Biology at Princeton University for instrument use and technical advice. Additionally, we would like to thank Lucy Reading-Ikkanda for figure design, Eric Wieschaus and Trudi Schüpbach for reagents and helpful comments, and members of the Streichan lab, as well as past and present members of the Shvartsman lab at Princeton and at the Flatiron institute for useful feedback and discussions. Stocks obtained from the Bloomington Drosophila Stock Center ( NIH P40OD018537 ) were used in this study.
Funding Information:
Research reported in this publication was supported by NIGMS of the NIH under grant number T32GM007388 (to Princeton Molecular Biology) andNIH Research Grant RO1GM134204(to S.Y.S.). We would like to thank Gary Laevsky and the Confocal Imaging Facility, a Nikon Center of Excellence, in the Department of Molecular Biology at Princeton University for instrument use and technical advice. Additionally, we would like to thank Lucy Reading-Ikkanda for figure design, Eric Wieschaus and Trudi Schüpbach for reagents and helpful comments, and members of the Streichan lab, as well as past and present members of the Shvartsman lab at Princeton and at the Flatiron institute for useful feedback and discussions. Stocks obtained from the Bloomington Drosophila Stock Center (NIH P40OD018537) were used in this study. C.M.S. performed experiments and wrote the manuscript. S.D. performed computational analysis of experimental data. V.J.-S. contributed code for analysis of left-right fluctuations in Figure 4. S.J.S. advised on analysis and experimental design. S.Y.S advised on analysis and experimental design, procured funding for the research, and advised on manuscript writing. All authors helped review the manuscript. The authors declare no competing interests.
Publisher Copyright:
© 2023 Elsevier Inc.
PY - 2023/8/21
Y1 - 2023/8/21
N2 - 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,1 but how this symmetry is maintained throughout subsequent morphogenetic events remains largely unknown.2 Here we show that the terminal patterning system—which relies on Ras/ERK signaling through activation of the Torso receptor by its ligand Trunk3—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.4 We 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,5 which reflects dramatic reorganization of global tissue flow and is incompatible with viability. Our 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.
AB - 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,1 but how this symmetry is maintained throughout subsequent morphogenetic events remains largely unknown.2 Here we show that the terminal patterning system—which relies on Ras/ERK signaling through activation of the Torso receptor by its ligand Trunk3—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.4 We 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,5 which reflects dramatic reorganization of global tissue flow and is incompatible with viability. Our 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.
UR - http://www.scopus.com/inward/record.url?scp=85167978833&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85167978833&partnerID=8YFLogxK
U2 - 10.1016/j.cub.2023.07.050
DO - 10.1016/j.cub.2023.07.050
M3 - Article
C2 - 37562404
AN - SCOPUS:85167978833
SN - 0960-9822
VL - 33
SP - 3536-3543.e6
JO - Current Biology
JF - Current Biology
IS - 16
ER -