The cytology of the vitellogenic stages of oogenesis in Drosophila melanogaster. I. General staging characteristics

Abstract

The cytology of the vitellogenic stages in the development of the oocyte of Drosophila melanogaster has been studied using whole mounts and sections of plastic-embedded ovaries and single egg chambers for light microscopy and cytochemistry. The migrations, changes in morphology, and synthetic products of the follicle cells are described as a function of developmental stage. The follicle cells synthesize the egg coverings, the vitelline and chorionic membranes, and elaborate the micropyle and dorsal chorionic appendages. The changing structure of the nurse cell nucleus and changes in organelle composition of its cytoplasm are described. The nurse cells synthesize ribosomes, lipid droplets, and mitochondria. These components pass through the ring canal system into the oocytc, which increases in volume some 200,000 times during its 78 hours of development.In mcst advanced, holometabolous insects possessing polytrophic, meroistic ovarioles, lhe oocyte is one of a group of inter-connected cells which is, in turn, surrounded by an envelope of follicle cells. The other cells of the cluster, the nurse cells, function in supplying nutrients to the oocyte (Snodgrass, ' 3 5 ) . In Drosophila melanogaster, as in most Diptera belonging to the superfamily Muscoidea, each egg chamber consists of a n oocyte and 15 nurse cells surrounded by a follicular envelope one cell thick. The egg and its 15 interconnected nurse cells are fourth generation descendants of a single cell, the germarial cystoblast. The interconnected cells formed by the division of a cystoblast are called cystocytes. It is within the germarium that the consecutive divisions occur which produce the sixteen cell cluster, and it is here also that the cluster becomes enveloped by the follicle cells. However, the major growth of the oocyte and its accompanying cells occurs within the vitellarium (Brown and King, '64). The main body of research on oogenesis in Drosophila has concentrated on the early stages in the formation and development of the oocyte. Much of this work has been reviewed by King ('64). The formation of the egg chamber in the germarial portion of the Drosophila ovariole and the system J. MORFH., 128: 427-442.of ring canals connecting nurse cells and oocyte within the egg chamber has been described by Brown and King ('64), and by Koch and King ('66). Subsequent work has been concerncd with identifying the mechanism which differentiates the oocyte from the sister nurse cells (Koch, Smith and King, '67). The role of the nurse cells in vitellogenesis has been investigated in nutritional studies (King and Sang, '59; Sang and King, '61). A few studies of limited scope have been concerned with cataloging organelles which flow from nurse cells into the egg, (King and Mills, '62), or which arise in the oocyte (Mahowald, '62, '68; Ullmann, '65). Some information is available concerning the composition of organelles found in the ooplasm during late developmental stages in Drosophila, (King, Bentley and Aggarwal, '66), and of the macromolecular changes ...

The song of the old mother: Reproductive senescence in female drosophila

“…The egg chamber leaves the germarium and moves down (proximally) the ovariole while undergoing vitellogenesis and further differentiation. 22,63,64 Oogenesis is subdivided into 14 distinct morphological stages, grouped into 2 major phases: previtellogenic (stages 2-6) and vitellogenic (stages 8-14) phases. 22,63 Both phases can be adversely affected by increasing female age.…”

“…22,63,64 Oogenesis is subdivided into 14 distinct morphological stages, grouped into 2 major phases: previtellogenic (stages 2-6) and vitellogenic (stages 8-14) phases. 22,63 Both phases can be adversely affected by increasing female age. In a study of females derived from a recently field-caught population, ovaries from aging or newly dead females contained a limited number of mature oocytes, but no other vitellogenic oocytes beyond the early stages 8/9 ( 15 , although the increasing age of experimental males potentially impacts this result).…”

A central role for microtubules in the differentiation of Drosophila oocytes

“…Egg chambers mature as they move through the ovariole, and have been divided into 14 morphologically distinct stages (Cummings and King, 1969). The present study addresses cytoskeletal organization and function through stage 5.…”

Male contributions to egg production: the role of accessory gland products and sperm inDrosophila melanogaster

“…Each of the two ovaries is made up of 16 AE1 ovarioles; each ovariole produces up to two mature oocytes daily. Several control points and feedback mechanisms regulate the production of a mature oocyte, a process that is divided into 14 stages (King et al 1956;Cummings & King 1969;Margaritis 1985;reviewed in King 1970;Spradling 1993). During the ¢rst seven oogenic stages (pre-vitellogenic stages) the oocyte and its nurse cells grow at similar rates.…”