Germ cell cysts and simultaneous sperm and oocyte production in a hermaphroditic nematode.

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.

A Sterile 20 Family Kinase and Its Co-factor CCM-3 Regulate Contractile Ring Proteins on Germline Intercellular Bridges.

Germ cells in most animals are connected by intercellular bridges, actin-based rings that form stable cytoplasmic connections between cells promoting communication and coordination [1]. Moreover, these connections are required for fertility [1, 2]. Intercellular bridges are proposed to arise from stabilization of the cytokinetic ring during incomplete cytokinesis [1]. Paradoxically, proteins that promote closure of cytokinetic rings are enriched on stably open intercellular bridges [1, 3, 4]. Given this inconsistency, the mechanism of intercellular bridge stabilization is unclear. Here, we used the C. elegans germline as a model for identifying molecular mechanisms regulating intercellular bridges. We report that bridges are actually highly dynamic, changing size at precise times during germ cell development. We focused on the regulation of bridge stability by anillins, key regulators of cytokinetic rings and cytoplasmic bridges [1, 4-7]. We identified GCK-1, a conserved serine/threonine kinase [8], as a putative novel anillin interactor. GCK-1 works together with CCM-3, a known binding partner [9], to promote intercellular bridge stability and limit localization of both canonical anillin and non-muscle myosin II (NMM-II) to intercellular bridges. Additionally, we found that a shorter anillin, known to stabilize bridges [4, 7], also regulates NMM-II levels at bridges. Consistent with these results, negative regulators of NMM-II stabilize intercellular bridges in the Drosophila egg chamber [10, 11]. Together with our findings, this suggests that tuning of myosin levels is a conserved mechanism for the stabilization of intercellular bridges that can occur by diverse molecular mechanisms.