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Intercellular bridges are proposed to arise from stabilization of a mitotic cytokinetic ring. Rehain-Bell et al. demonstrate that inhibition of non-muscle myosin II is a conserved mechanism of bridge stabilization and find that, in the C. elegans oogenic germline, this is mediated by GCK-1Ste-20 Kinase, its co-factor CCM-3, and anillin proteins.
Studies of gamete development in the self-fertile hermaphrodites of Caenorhabditis elegans have significantly contributed to our understanding of fundamental developmental mechanisms. However, evolutionary transitions from outcrossing males and females to self-fertile hermaphrodites have convergently evolved within multiple nematode sub-lineages, and whether the C. elegans pattern of self-fertile hermaphroditism and gamete development is representative remains largely unexplored. Here we describe a pattern of sperm production in the trioecious (male/female/hermaphrodite) nematode Rhabditis sp. SB347 (recently named Auanema rhodensis) that differs from C. elegans in two striking ways. First, while C. elegans hermaphrodites make a one-time switch from sperm to oocyte production, R. sp. SB347 hermaphrodites continuously produce both sperm and oocytes. Secondly, while C. elegans germ cell proliferation is limited to germline stem cells (GSCs), sperm production in R. sp. SB347 includes an additional population of mitotically dividing cells that are a developmental intermediate between GSCs and fully differentiated spermatocytes. These cells are present in males and hermaphrodites but not females, and exhibit key characteristics of spermatogonia - the mitotic progenitors of spermatocytes in flies and vertebrates. Specifically, they exist outside the stem cell niche, increase germ cell numbers by transit-amplifying divisions, and synchronously proliferate within germ cell cysts. We also discovered spermatogonia in other trioecious Rhabditis species, but not in the male/female species Rhabditis axei or the more distant hermaphroditic Oscheius tipulae. The discovery of simultaneous hermaphroditism and spermatogonia in a lab-cultivatable nematode suggests R. sp. SB347 as a richly informative species for comparative studies of gametogenesis.
Actomyosin-driven cortical contractility is a hallmark of many biological processes. While most attention has been given to the positive regulation of contractility, it is becoming increasingly appreciated that contractility is also limited by negative regulation and mechanical brakes. The cytokinetic ring is an actomyosin contractile structure whose assembly and constriction are activated by the small GTPase RhoA. Here we describe the role of two novel cytokinetic ring components GCK-1 and CCM-3 in inhibiting contractility in the cytokinetic ring. GCK-1 and CCM-3 co-localize with essential cytokinetic ring proteins such as active RhoA, the scaffold protein anillin and non-muscle myosin II (NMM-II) during anaphase. GCK-1 and CCM-3 are interdependent for their localization and require active RhoA and anillin but not NMM-II for their recruitment to the cytokinetic furrow. Partial depletion of either GCK-1 or CCM-3 leads to an increase of active RhoA, anillin and NMM-II in the cytokinetic furrow and increased rates of furrow ingression. Furthermore, GCK-1 and CCM-3 localize to actomyosin foci during pulsed contractility of the cortical cytoskeleton during zygote polarization. Depletion of GCK-1 or CCM-3 leads to an increase in both cortical contractility and baseline active RhoA levels. Together, our findings suggest that GCK-1 and CCM-3 limit contractility during zygote polarization and
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