Ultrastructural features of the trophonema and oogenesis in the starlet sea anemone, Nematostella vectensis (Edwardsiidae)

Abstract

Abstract. The starlet sea anemone, Nematostella vectensis Stephenson 1935, is a burrowing, estuarine species that has become a model organism for fundamental studies of cnidarian and metazoan development. During early oogenesis, oocytes appear in the basal region of the gastrodermis in the reproductive mesenteries and gradually bulge into the adjacent connective tissue space (mesoglea) where the majority of oocyte growth and vitellogenesis occurs. However, oocytes do not physically contact the cellular and amorphous matrix of the mesogleal compartment due to a thin, intervening basal lamina. Oocytes retain limited contact with the basal gastrodermal epithelium via groups of ultrastructurally modified gastrodermal cells called trophocytes. Trophocytes are monociliated accessory cells of somatic origin that collectively form a structure called the trophonema, a unique accessory cell/oocyte association not observed outside the Cnidaria. The trophonema consists of 50–60 trophocytes that maintain contact with <1% of the oocyte surface and forms a circular, bowel‐shaped depression on the luminal surface of the gastrodermis as they sink into the mesoglea with the oocyte. The oocyte remains highly polarized throughout oogenesis with the germinal vesicle positioned near the trophonema and presumably representing the future animal pole of the embryo. Contact between the trophonema and the oocyte is restricted to cell junctions connecting peripheral trophocytes and narrow extensions from the oocyte. Previous studies suggest that the trophonema plays a role in transport of extracellular digestive products from the gastrovascular cavity to the oocyte, and the ultrastructural features described in this study are consistent with that view. Vitellogenesis is described for the first time in a sea anemone. Yolk synthesis involves both autosynthetic and heterosynthetic processes including the biosynthetic activity of the Golgi complex and the uptake of extraoocytic yolk precursors via endocytosis, respectively.

The embryonic development of the cnidarianHydractinia echinata

“…, H and K). Very similar granules were described as yolk in the oocytes of other cnidarians (Larkman ; Eckelbarger et al ). This layer also contains lipid droplets (Fig.…”

Gametogenesis and reproductive periodicity of the “biologically vulnerable” giant Caribbean sea anemone, Condylactis gigantea, in Florida

“…The process of gametogenesis is similar to that in many other actiniarians (e.g., Dunn ; Wedi & Dunn ; Shick ; Fautin ; Eckelbarger et al. ; Scott & Harrison ). Jennison () documented trophonemata associated with oocytes of C. gigantea , but trophonemata in association with spermaries of this species (see Fig.…”

“…It has been proposed that a trophonema delivers nutrients from the gastrovascular cavity to a developing germ cell (Larkman & Carter ; Eckelbarger et al. ), and functions in the release of gametes from mesenteries at spawning (Carter & Miles ; Scott & Harrison ).…”

The making of an embryo in a basal metazoan: Proteomic analysis in the sea anemone Nematostella vectensis

“…In addition, ZP‐containing proteins mediate the polymerization of proteins into fibrils or matrices . The Nematostella oocyte has no vitelline membrane and fertilization is not affected when the jelly sac is removed; thus, this protein might contribute to the polymerization of the jelly matrix.…”

“…The genome sequence of the starlet sea anemone Nematostella vectensis provides molecular information which enables more comprehensive studies in Cnidaria. An ultrastructural study of the anemone has provided a detailed description of the oocyte subcellular organization during oogenesis . In addition, we have recently characterized the proteomic profile of Nematostella ovulated mature oocyte, identifying more than 1500 proteins that are involved in oocyte metabolism, regulation and RNA silencing .…”