Soma–Germ Cell Interactions inCaenorhabditis elegans:Multiple Events of Hermaphrodite Germline Development Require the Somatic Sheath and Spermathecal Lineages

Abstract

Germ cells complete multiple events to form functional oocytes and sperm. In the Caenorhabditis elegans hermaphrodite, germ cells develop in proximity to the somatic gonad sheath and spermathecal cells. We present evidence from cellular laser ablation studies indicating that cells of the somatic sheath and spermathecal lineages play critical roles in four events of hermaphrodite germline development. (1) Cells of the sheath and spermathecal lineage support germline proliferation; ablation of sheath/spermathecal precursor cells reduces mitotic proliferation. (2) These cells also play a role in the exit of germ cells from the pachytene stage of meiotic prophase and/or gamete differentiation; ablation can result in undifferentiated germ cells arrested in pachytene. (3) Proximal sheath and distal spermatheca cells are required for ovulation of the oocyte. During wild-type ovulation, the mature oocyte is expelled from the gonad arm by contraction of the proximal myoepithelial sheath and dilation of the distal spermatheca. Ablation of these cells traps mature oocytes in the gonad arm where they endomitotically replicate their DNA (the Emo phenotype). (4) Cells of the sheath and spermathecal lineage also appear to promote the male germ cell fate since ablation of one sheath/spermathecal precursor cell can feminize the hermaphrodite germ line. These somatic ablation-induced germline phenotypes demonstrate that the somatic gonad is required for multiple events in C. elegans germline development. Further, these results suggest that soma to germline cell-cell interactions in C. elegans are physiological in character (i.e., contraction during ovulation) as well as regulatory.

Structural components of the nonstriated contractile apparatuses in the Caenorhabditis elegans gonadal myoepithelial sheath and their essential roles for ovulation

“…When ovulation fails, a mature oocyte remains in the proximal ovary, repeats DNA synthesis without cell division, and becomes endomitotic (Iwasaki et al, 1996;McCarter et al, 1997McCarter et al, , 1999. This phenotype is designated as Emo (endomytotic oocytes in the proximal ovary) and is characterized by intense staining by 4Ј6-diamidino-2-phenylindole, dihydrochloride (DAPI) of overly amplified nuclear DNA in endomitotic oocytes ( Fig.…”

“…1). The germline and oocytes are surrounded by 10 sheath cells (pairs 1-5), and ovulation requires a signal from sperm that induces ovarian contraction and oocyte maturation, which are then followed by dilation of the spermatheca and fertilization (Ward and Carrel, 1979;McCarter et al, 1997McCarter et al, , 1999Hubbard and Greenstein, 2000;Yamamoto et al, 2006). The proximal sheath cells (pairs 3-5; Fig.…”

“…1) are smooth musclelike cells with distinct thin and thick filaments and designated as the myoepithelial sheath (Hirsh et al, 1976;Strome, 1986;Ardizzi and Epstein, 1987;Hall et al, 1999). Contraction of the myoepithelial sheath is periodically enhanced upon maturation of the most proximal oocytes (McCarter et al, 1997(McCarter et al, , 1999. Sheath contraction is negatively regulated by ceh-18 encoding a POU-class homeoprotein (Rose et al, 1997;Miller et al, 2003) and gap junctions that are formed between the myoepithelial sheath and maturing oocytes (Whitten and Miller, 2006).…”

Caenorhabditis elegans germ line: A model for stem cell biology

“…An alternative explanation is that such mutations affect aspects of cell cycle control that are common to mitosis and meiosis causing cells to arrest in an intermediate state. Other mutations and non-DTC cell ablations can reduce germline proliferation even when all cells are in the mitotic cell cycle, as driven by hyperactive GLP-1 function (Hubbard et al, 1996;McCarter et al, 1997;Killian and Hubbard, 2005). These results indicate that optimal germline proliferation requires additional inputs that act in conjunction with GLP-1 signaling (Fig.…”

“…The germ line is the only C. elegans lineage that proliferates for the life of the organism (Hirsh et al, 1976). The maintenance of germ cell proliferation is governed by interaction with a niche, the distal tip cell (DTC; Kimble and White, 1981), while additional cell-cell communication contributes to the extent of germline proliferation (McCarter et al, 1997;Pepper et al, 2003;Killian and Hubbard, 2005). Finally, like mammalian stem cells, the C. elegans germ line appears to be quite plastic and responsive to changing molecular and physiological conditions.…”