Septins and a formin have distinct functions in anaphase chiral cortical rotation in theCaenorhabditis eleganszygote

Abstract

Many cells and tissues exhibit chirality that stems from the chirality of proteins and polymers. In the C. elegans zygote actomyosin contractility drives chiral rotation of the entire cortex circumferentially around the division plane during anaphase. How contractility is translated to cell-scale chirality, and what dictates handedness, are unknown. Septins are candidate contributors to cell-scale chirality because they anchor and crosslink the actomyosin cytoskeleton. We report that septins are required for anaphase cortical rotation. In contrast, the formin CYK-1, which we found to be enriched in the posterior in early anaphase, is not required for cortical rotation, but contributes to its chirality. Simultaneous loss of septin and CYK-1 function led to abnormal and often reversed cortical rotation. Our results suggest that anaphase contractility leads to chiral rotation by releasing torsional stress generated during formin-based polymerization, which is polarized along the cell anterior-posterior axis, and which accumulates due to actomyosin network connectivity. Our findings shed light on the molecular and physical bases for cellular chirality in the C. elegans zygote. We also identify conditions in which chiral rotation fails but animals are developmentally viable, opening avenues for future work on the relationship between early embryonic cellular chirality and animal body plan. [Media: see text] [Media: see text]

A cytokinetic ring-driven cell rotation achieves Hertwig’s rule in early development

“…S6 B and Movie S10 ) indicating that NMY-2/Myosin activity in the AB cell drives both a whole-cell and whole-embryo rotation. Together, this shows that the whole embryo is essentially free to rotate inside the eggshell, consistent with earlier observations ( 47 , 48 , 60 , 61 ).…”

Bending actin filaments: twists of fate

“…Intriguingly, α-Actinin, IQGAP, and unconventional myosins also induce directional actin filament movements such as counterclockwise swirling. This actin-dependent cell chirality is observed in a wide range of animals from Drosophila to mammals 57 , 111 , 114 – 121 . While much of the evidence for actin bending and its biological consequences to date comes from studies using in vitro systems, recent studies using cells and model organisms revealed that cell chirality has important roles in processes such as cell migration and L-R asymmetric organ development 97 , 106 , 122 , 123 .…”

Caenorhabditis elegans septins contribute to the development and structure of the oogenic germline

“…These strains are considered to be loss‐of‐function alleles due to the corresponding mRNA being undetectable by northern blotting, and protein undetectable by immunoblotting (Nguyen et al, 2000). We recently published that our strain bearing unc‐59(e1005) no longer contains Gly29‐to‐Arg29 but instead contains a different residue mutation (Gly54‐to‐Arg54; Zaatri et al, 2021), which disrupts the 5′ splice site consensus sequence (Riddle et al, 1997) in the intron between exon 1 and exon 2 of unc‐59 . While unc‐59(e1005) allele bearing Gly29‐to‐Arg29 and the unc‐61(e228) allele were previously reported to have postembryonic defects consistent with roles germline function, we wanted to validate and perform a detailed characterization of our unc‐59(e1005) allele bearing Gly54‐to‐Arg54.…”