Asymmetrical rotations of blastomeres in early cleavage of gastropoda

Abstract

The movements of blastomere surfaces marked with carbon particles during cytokinesis of the Ist-IVth cleavage divisions in the eggs of the gastropodsLymnaea stagnalis, L. palustris, Physa acuta and Ph. fontinalis have been studied by time-lapse cinematographic methods. The vitelline membrane was removed with trypsin. At 2- and 4-cell stages shifts of nuclei have also been studied.Symmetrical as well as asymmetrical surface movements (in respect to the furrow plane) have been revealed. Symmetrical surface movements at the beginning of cytokinesis consist mainly in contraction of the furrow zone and in expansion of the more peripheral regions; between these there is a stationary zone. After the end of cytokinesis the furrow region expands.Considerableasymmetrical surface movements have also been observed in all four divisions. From anaphase until the end of cytokinesis each of the two sister blastomeres rotates with respect to the other in such a way, that if viewed along the spindle axis, the blastomere nearest to the observer rotates dexiotropically in a dextral species and laeotropically in a sinistral species (primary rotations). After the completion of cytokinesis the blastomeres may rotate in a reverse direction. The latter rotations are less pronounced in the IInd and IIIrd divisions and most pronounced in the IVth division. Blastomeres with the vitelline membrane intact retain a slight capacity for primary rotations. In normal conditions nuclei of the first two blastomeres shift mainly laeotropically in dextral species, but dexiotropically in sinistral species, being carried along by the reverse surface rotations.The invariable primary asymmetrical rotations of blastomeres seem to be the basis of enantiomorphism in molluscan cleavage. They are assumed to be determined by an asymmetrical structure of the contractile ring carrying out the cytokinesis.

Far from solved: A perspective on what we know about early mechanisms of left–right asymmetry

“…LR asymmetry is established in some animals during early developmental stages, long before cilia are present or in some cases, with no cilia present at all; these include snails (Meshcheryakov and Beloussov, 1975;Shibazaki et al, 2004), sea urchin (Kitazawa and Amemiya, 2007), Drosophila (Hozumi et al, 2006;Coutelis et al, 2008), Arabidopsis (Hashimoto, 2002;Thitamadee et al, 2002;Abe et al, 2004), and C. elegans (Priess, 1994;Hutter and Schnabel, 1995), for example. Other animals establish the LR axis later in development, when thousands of cells are present, but also without using cilia.…”

“…Just as mRNAs and proteins have been shown to be differentially distributed to daughter cells, this model proposes that selective imprinting of chromosomes is a means of achieving asymmetries on the left and right side. Differential chromatid segregation is well-studied in yeast (Armakolas et al, 2010), and early cleavages in some animals, such as snails, are determined by the asymmetric structure of a contractile ring carrying out cytokinesis (Meshcheryakov and Beloussov, 1975). The discovery of a role for the motor protein left-right Dynein in this process is also extremely suggestive (Armakolas and Klar, 2007).…”

A twisting story: how a single gene twists a snail? Mechanogenetics

“…We also observed that sinistral embryos occasionally showed dextral-type blastomere arrangement at the four-cell stage even inside the egg capsules, but they showed normal counterclockwise cleavage at the third division (Kuroda et al 2009). It was reported that chirality is distinguishable as early as the second or even the first cleavage (Meshcheryakov & Beloussov, 1975); however, our micromanipulation experiments have proven that the macromere-micromere cell contacts at the eight-cell stage embryo is the first determining step for asymmetric development.…”

Spiral cleavages determine the left-right body plan by regulating Nodal pathway in monomorphic gastropods, Physa acuta

“…The rotation direction of protruding micromeres is always referred as looking down from the animal pole. It had been believed that all the developmental steps for the sinistral and dextral embryos are mirror images of each other based on conventional microscopic observations (Crampton, 1894;Meshcheryakov and Beloussov, 1975). However, by close analysis of the temporal and spatial behaviour of cytoskeletons of the dextral and the sinistral L. stagnalis during the early cleavages, we have revealed non-mirrorimage cytoskeletal dynamics at the third cleavage (Shibazaki et al, 2004).…”

“…Spiral cleavage where the cleavage planes are at oblique angles to the animal-vegetal axis of the egg occurs during the second (or may be even the first?) to fifth cleavages in alternating rotation direction, but they are most notable during the third to fifth cleavages (Meshcheryakov, 1975;Verdonk and van den Biggelaar, 1983;Lambert, 2010). Embryos manually forced to rotate clockwise way at the third cleavage opposite to the wild type, underwent anticlockwise rotation first during the macromere division and then during the micromere division as well, in the subsequent fourth cleavage.…”