Origin, fate, and function of the components of the avian germ disc region and early blastoderm: Role of ooplasmic determinants

Abstract

In the avian oocytal germ disc region, at the end of oogenesis, we discerned four ooplasms (␣, ␤, ␥, ␦) presenting an onion-peel distribution (from peripheral and superficial to central and deep. Their fate was followed during early embryonic development. The most superficial and peripheral ␣ ooplasm plays a fundamental role during cleavage. The ␤ ooplasm, originally localized in the peripheral region of the blastodisc, becomes mainly concentrated in the primitive streak. At the moment of bilateral symmetrization, a spatially oblique, sickle-shaped uptake of ␥ and ␦ ooplasms occurs so that ␥ and ␦ ooplasms become incorporated into the deeper part of the avian blastoderm. These ooplasms seem to contain ooplasmic determinants that initiate either early neurulation or gastrulation events. The early neural plate-inducing structure that forms a deep part of the blastoderm is the ␦ ooplasm-containing endophyll (primary hypoblast). Together with the primordial germ cells, it is derived from the superficial centrocaudal part of the nucleus of Pander, which also contains ␦ ooplasm. The other structure (␥ ooplasm) that is incorporated into the caudolateral deep part of the blastoderm forms Rauber's sickle. It induces gastrulation in the concavity of Rauber's sickle and blood island formation exterior to Rauber's sickle. Rauber's sickle develops by ingrowth of blastodermal cells into the ␥ ooplasm, which surrounds the nucleus of Pander. Rauber's sickle constitutes the primary major organizer of the avian blastoderm and generates only extraembryonic tissues (junctional and sickle endoblast). By imparting positional information, it organizes and dominates the whole blastoderm (controlling gastrulation, neurulation, and coelom and cardiovascular system formation). Fragments of the horns of Rauber's sickle extend far cranially into the lateral quadrants of the unincubated blastoderm, so that often Rauber's sickle material forms three quarters of a circle. This finding explains the regulative capacities of isolated blastoderm parts, with the exception of the anti-sickle region and central blastoderm region, where no Rauber's sickle material is present. In avian blastoderms, there exists a competitive inhibition by Rauber's sickle on the primitive streak and neural plate-inducing effects of sickle endoblast. Avian primordial germ cells contain ␦ ooplasm derived from the superficial part of the nucleus of Pander. Their original deep and central ooplasmic localization has been confirmed by the use of a chicken vasa homologue. We conclude that the unincubated blastoderm consists of three elementary tissues: upper layer mainly containing ␤ ooplasm, endophyll containing ␦ ooplasm, and Rauber's sickle containing ␥ ooplasm). These elementary tissues form before the three classic germ layers have developed.

August Rauber (1841-1917): from the primitive streak to Cellularmechanik

“…Indeed, the lunulashaped region of the epiblast giving rise to the primitive streak is still referred to as 'Rauber's sickle' (Rauber 1875b(Rauber , 1876aCallebaut and Van Nueten 1994). Most recent data corroborate Rauber's conclusion when relating 'Rauber's sickle' to the gastrulation organizer of the avian blastoderm (Callebaut 2005(Callebaut : 1203 cf. Lawson and Schoenwolf 2003).…”

Mosaic versus regulation development in avian blastoderms depends on the spatial distribution of Rauber's sickle material

“…In our present study, we have demonstrated that in the same species (Gallus domesticus) and the same blastoderm both mosaic development or regulation phenomena can be obtained, only by the different geometric distribution of Rauber's sickle material in the isolated blastoderm fragment. Rauber's sickle material that contains g ooplasm (Callebaut, 1994(Callebaut, , 2005, regulates early embryonic patterning (gastrulation) by its inducing effect on the upper layer Fig. 6.…”

“…Stereomicroscopic Polaroid photographs were taken in the same direction at the beginning, during, and at the end of the culture period. Fixation and embedding in paraffin were performed as mentioned in earlier studies (Callebaut, 2005).…”

“…Our knowledge about the origin, fate, and function of different elements of the avian germ disc region has improved only recently (Callebaut 1993a(Callebaut -c, 1994(Callebaut , 2005Van Nueten, 1994, 1995;Callebaut et al, 1999Callebaut et al, , 2000Callebaut et al, , 2003.…”

Germline development in amniotes: A paradigm shift in primordial germ cell specification

“…Therefore, it would be reasonable to think that induction would be the modality adopted in PGC specification in avian embryos. Despite this regulative capacity, it was proposed that different ‘ooplasms’ (maternally derived substances present in the egg cell), localised in different regions of the mature oocyte, are inherited by different portions of the developing embryo: pPGCs would inherit the so‐called ‘δ ooplasm’, localised in the deep central area 67, 68. This was the first support of what became the current view on PGC specification in the avian embryo: maternally produced germ plasm determines PGCs.…”