Fine Structures of Oocytes and Accessory Cells of the Ovary in the Starfish Patiria (Asterina) pectinifera at Different Stages of Oogenesis and After 1‐Methyladenine‐Induced Maturation

Abstract

Morphological changes in the growing and maturing oocytes of Patiria (Asterina) pectinifera were studied by electron microscopy.An extensive system of rough endoplasmic reticulum (ER) and Golgi complex (GC) develops in the ooplasm forming the cortical, yolk and secretory granules in its peripheral regions. The contents of the latter granules are released from the oocyte and form the vitelline membrane. At early stages of oogenesis, extensive multiplication of mitochondria results in formation of a large aggregate of these organelles in the perinuclear cytoplasm ("yolk nucleus"). After maturation of full grown oocytes has been induced by 1-methyladenine, the membranous cell structures are rapidly rearranged : vast aggregates of ER cisternae in the surface cytoplasm layer and single ER cisternae among yolk granules are disintegrated to small vesicles; the GC is reduced. These processes are suggested to be somehow related to changes in hydration of the cytoplasm and in rigidity of its surface layer. In maturing oocytes, the yolk granules form characteristic linear rows, trabeculae, traversing the cytoplasm and their boundary membranes fuse in zones of contact. Some granules are converted to multivesicular bodies, thus suggesting the activation of hydrolytic enzymes that form part of the yolk in echinoderms.Oogenesis is of the solitary type.In 1969, KANATANI first showed (1) that radial nerve extracts of starfish induced synthesis and secretion of 1-methyladenine (1-MA) by the follicle cells. These cells contract and seem to push the oocytes out of the ovary (2). 1-MA acts on the oocyte surface and induces the formation of maturation-promoting factor in the cytoplasm that causes breakdown of the germinal vesicle and oocyte maturation (3).Within 15 years after this discovery by KANATANI a great number of papers were published dealing with the physiological and molecular mechanisms of maturation (for review, see 3-5). But there have been few morphological studies on starfish oocytes at different stages of growth and maturation, apparently due to the absence of appropriate fixatives for echinoderms suitable for electron microscopic studies.The information obtained on structural changes in the oocytes during this period is essentially as follows. Within the first five minutes after treatment of full grown oocytes with 1-MA, the rigidity of the surface layer of the cytoplasm markedly decreases (6, 7). Microvilli

Ovarian ultrastructure and vitellogenesis in ten species of shallow-water and bathyal sea cucumbers (Echinodermata: Holothuroidea)

“…In the present study the Golgi complex and RER appeared to play an important role in the assemblage of yolk bodies in the oocytes of every species we examined, indicating that the oocytes play a significant role in vitellogenesis. Extensive arrays of RER cisternae are commonly observed in the ooplasm of vitellogenic oocytes in many echinoderms (Kessel, 1964(Kessel, ,1968Chatlynne, 1972;Piatiagorsky, 1975;Ferrand, 1984;Aisenshtadt & Vassetzky, 1986) and numerous other invertebrate groups (N0rrevang, 1968;Anderson, 1974;Eckelbarger, 1984;Wourrns, 1987), but were very restricted in the oocytes of all the holothuroid species we examined. Byrne (1989) noted a similar paucity of RER cisternae in the oocytes of the ophiuroid Ophiolepis paucispina.…”

“…However, relatively little is known of the ultrastructural features of oogenesis and of vitellogenesis in particular. Most studies of oogenesis have concentrated on asteroids and echinoids (Piatagorsky, 1975;Walker, 1982;Kanatani & Nagahama, 1983;Beijnink et al, 1984;Ferrand, 1984;Aisenshtadt & Vassetzky, 1986) with only a few published reports on two species of ophiuroids (Kessel, 1968;Byrne, 1988Byrne, ,1989 and two species of holothuroids (Kessel, 1964;Smiley & Cloney, 1985;Smiley, 1988Smiley, ,1990Smiley et al, 1991). No studies have been conducted on the ultrastructural features of the ovary or oogenesis in any deep-sea echinoderm.…”

Reproduction inBathyplotes natans(Holothurioidea: Synallactidae) from bathyal depths in the north-east and western Atlantic

“…Yolk synthesis appears to involve the autosynthetic activity of the Golgi complex and RER, although ultrastructural studies alone will not rule out the possible transport of yolk precursors from extraovarian sources. The extensive arrays of RER cisternae frequently reported from the oocytes of other echinoderms (Piatiagorsky, 1975;Ferrand, 1984;Aisenshtadt & Vassetzky, 1986) are largely absent in holothuroid oocytes (Eckelbarger & Young, 1992). Endocytotic activity, potentially related to the uptake of extraovarian precursors, varies widely in holothuroids, with high levels being observed in the vitellogenic oocytes of some species and low-level activity in others (Eckelbarger & Young, 1992).…”

Allelic inheritance in naturally occurring parthenogenetic offspring of the gonochoric sea star Patiria miniata

“…Examples of natural parthenogenesis (e.g., Yamaguchi & Lucas 1984) are rare among echinoderms, but artificial induction of parthenogenesis in gonochoric outcrossing sea stars has been widely used in studies of cell cycle control, intracellular signalling, and egg activation (e.g., Hamaguchi 2001; Sasaki & Chiba 2004; Mita 2005; Mori et al 2006). One inducer of parthenogenetic sea star development is 1‐methyladenine (1‐MA), which is released by sea star ovarian follicle cells in nature to induce the resumption of meiosis and maturation of oocytes, and can be used in vitro to induce ovulation and spawning behavior (Doreé & Guerrier 1975; Picard & Doreé 1983; Aisenshtadt & Vassetzky 1986; Strathmann 1987; Yoshikuni et al 1988).…”

“…One inducer of parthenogenetic sea star development is 1-methyladenine (1-MA), which is released by sea star ovarian follicle cells in nature to induce the resumption of meiosis and maturation of oocytes, and can be used in vitro to induce ovulation and spawning behavior (Doree´& Guerrier 1975;Picard & Doree1 983;Aisenshtadt & Vassetzky 1986;Strathmann 1987;Yoshikuni et al 1988). The earliest reports of sea star parthenogenesis in California populations of Patiria miniata BRANDT 1835, by Loeb (1913) and Newman (1921), predate the discovery of the hormonal basis of sea star oocyte maturation.…”