Ascidian follicle cells: Multifunctional adjuncts to maturation and development

Abstract

Ascidians are primitive chordates, subphylum Tunicata, that are sessile filter-feeding hermaphrodites as adults. Released oocytes are enclosed within a monolayer of follicle cells, a non-cellular vitelline coat and a monolayer of test cells that cover the egg membrane. Follicle cell structure is distinctive in different groups. They originate from circulating hemoblasts with functional nuclei. They are necessary for germinal vesicle breakdown in several species and may secrete a meiosis-inducing substance to the oocyte. In some families the follicle cells are necessary for fertilization. Although all ascidians are hermaphrodites, many are not capable of self fertilization. The follicle cells seem to be involved in self, non-self discrimination. Attachment of sperm to egg involves a sperm surface glycosidase binding to an egg surface glycoside. The primary block to polyspermy involves a glycosidase released by the follicle cells. In one species with direct development, the follicle cells secrete a sticky substance that anchors the embryos in a wave-swept rocky area; a brooding solitary ascidian with a tadpole larva uses a sticky substance secreted by follicle cells to attach the brood to the atrial chamber. Several species have floating eggs due to buoyancy of their follicle cells, a result of ammonia sequestration in at least one species. Many other marine invertebrates release eggs with attached follicle cells, and all vertebrates ovulate oocytes covered with follicle cells. Comparisons are discussed between these groups and ascidians.

In the ovary of Ciona intestinalis (Type A), immune-related galectin and phenoloxidase genes are differentially expressed by the follicle accessory cells

“…The dynamic of the FC layer morphogenesis has been related to a nonproliferative process [62], so a putative effect of CiLgals as proliferation stimulus can be excluded, whereas a modulatory effect on FCs differentiation cannot be excluded [63]. Presumably due to the used histological method and/or the cutting level of the sections, we were not able to distinguish two FC layers (inner and outer) [49,52], moreover, these two layers have not been described by the previous electron microscopy study on C. intestinalis from the Mediterranean Sea [48].…”

“…The ovary consists of a branched ovarian tube and follicles formed by growing oocytes encased by their accessory cells [46]. The ovary follicles are usually distinguished in three stages: young oocyte of smaller size in which the accessory cells layers may be incomplete (stage I); vitellogenic (stage II) and post-vitellogenic (stage III) follicles which are formed by the oocyte-accessory cells complex [47][48][49]. According to a transmission electron microscopy study by Mancuso [48], the C. intestinalis (type A) ovarian follicles at vitellogenic and post-vitellogenic stages are composed of two maternal accessory cell types which surround the oocytes: follicle cells (outer layer, FCs), and test cells (inner layer, TCs) which are in contact with the oocyte membrane.…”

Early biotic interactions among introduced and native benthic species reveal cryptic predation and shifts in larval behaviour

“…Even though fertilization is species-specific in most ascidians, in solitary species heterologous sperm can trigger mechanisms that block polyspermy, hindering subsequent fertilization by homologous sperm (Lambert 2001). Follicle cells enveloping the eggs are involved in the fertilization process and in the establishment of this primary block to polyspermy in response to conspecific and heterospecific sperm (Lambert 2009). This process did not seem to act in the present work.…”

Obtaining Gametes and Embryos of Ascidians

“…All ascidians are hermaphroditic; some are protandric, but most are simultaneous hermaphrodites. Selffertilization is possible in some species, but many are self-sterile [ 2 ]. The ascidians include three orders: Aplousobranchia, Phlebobranchia, and Stolidobranchia [ 3 ].…”