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

Abstract

Oocytes must be exceptionally large cells in order to support embryonic development. Throughout animal phylogeny, a specialized cell called a syncytium, wherein many nuclei share a continuous cytoplasm, achieves oogenesis. The syncytial nature of germline architecture is key to its function and depends on conserved components of the cortical cytoskeleton. Septins form non‐polar cytoskeletal polymers that associate with membranes. In the syncytial germline of the nematode Caenorhabditis elegans, septins are highly enriched on the cortex and generally required for fertility, but the role of septins in the germline is poorly understood. We report that the C. elegans septins, UNC‐59 and UNC‐61, are important for germline extension during development, the maintenance of its syncytial architecture, and production of oocytes. While much of our findings substantiate the idea that the two C. elegans septins act together, we also found evidence that they have distinct functions. Loss of UNC‐61 perturbed germline extension during germline development, while the loss of UNC‐59 function severely affected germline architecture in adult hermaphrodites. Consultation of clustering results from a large‐scale high‐throughput screen suggested that septins are involved in germ cell proliferation and/or differentiation. In sum, our findings implicate a conserved cytoskeletal component in the complex architecture of a germline syncytium.

Septins throughout phylogeny are predicted to have a transmembrane domain, which inCaenorhabditis elegansis functionally important

“…For example, an O-glycan is highly enriched on the vulval lumen and under the flaps of cu�cle that flank the vulval slit, in two half-circles where UNC-61a is uniquely enriched 64,65 . Abnormal vulval opening may explain the germline extrusion phenotype of loss of sep�n func�on in C. elegans 23,25 .…”

“…C. elegans fluorescence imaging was performed as previously described 25 . Whole worm images were acquired using a Nikon A1R microscope with a 60 × 1.27 NA Nikon water immersion objective with a gallium arsenide phosphide photo-multiplier tube (GaAsP PMT) using NIS-Elements software.…”

“…These two sep�ns exhibit behaviors shared by other organisms' sep�ns, including enrichment in and requirement for normal func�on of the cytokine�c ring 22,23,[39][40][41] . Loss of sep�n func�on in C. elegans also leads to morphological defects of the C. elegans syncy�al germline and reduced fer�lity [23][24][25][26] . While the C. elegans sep�ns have been considered as a two-protein system, in fact, one of the C. elegans sep�n genes, unc-61, encodes three isoforms: a, b, and c (Figure 2A).…”

“…The C. elegans sep�ns localize similarly to core sep�ns in other organisms, including to the cytokine�c ring 23,24 . Loss of sep�n func�on results in several phenotypes, including uncoordinated movement, germline extrusion, and vulval protrusion, that occur in well studied �ssues, like the vulva, but the role of sep�ns in these �ssues remains unclear 23,25,26 .…”

Introduction to the Special Issue of Cytoskeleton on the molecular and cell biology of septins

“…Benson and McMurray (2023) work with S. cerevisiae septins Cdc3 and Cdc10 to suggest what may restrict septin localisation to specific membranes. Perry et al (2023) study C. elegans septins UNC‐59 and UNC‐61, implicate septins in the architecture of the germline syncytium (where many germs cells share a common cytoplasm), and propose different roles for the two different septins. Kim et al (2023) discuss the role of septins and actin at endothelial cell–cell junctions and how they impact monolayer integrity.…”