Worm Breeder's Gazette 9(2): 64

These abstracts should not be cited in bibliographies. Material contained herein should be treated as personal communication and should be cited as such only with the consent of the author.

Reversal of Cell Division Polarity and Early Cell-Cell Interaction in the Embryo of C. elegans

E. Schierenberg

During early embryogenesis of C.  elegans the serial stemcell-like 
cleavages of the germline cells P0-P3 generate a number of somatic 
founder cells with different developmental potentials.  Observations 
on partial embryos show that these four unequal divisions occur 
orthogonal to the anterior-posterior axis of the egg.  In the first 
two of these germline divisions the somatic daughter cell comes to lie 
anterior to the new germline cell.  In the following two, however, the 
somatic daughter comes to lie posterior, suggesting a reversal of 
polarity in the germline.  By the use of a laser microbeam, egg 
fragments can be extruded from young embryos.  These fragments can 
develop like partial twins.  If the fragment is derived from the 
uncleaved zygote P0, its first division generates two P1-like cells.  
Further development reveals that the mirror image duplications are 
joined at their anterior poles.  If the fragment is derived from P1 
the first division generates two P2-like cells.  Further development 
reveals that here the duplications are joined at their posterior poles.
From this it is concluded that in fact a reversal of polarity takes 
place in the germline cell P2 as an integral part of normal 
development.  This notion is confirmed by the finding that partial 
embryos derived from the posterior region of P2 were not able to 
undergo germline-like cleavages in contrast to those derived from P0 
or P1.  Thus,polarity appears not to be a static feature but a dynamic 
property which is (or at least can be) newly established during each 
cell cycle in the early germline cells.  This view is in accordance 
with the behavior of the P-granules(Strome and Wood ,Cell 35 , 15-25 , 
1983 ).
What could be the developmental significance of this reversal 
phenomenon?  It may occur in order to preserve the contiguity between 
the intestinal precursors (E-cells) and the germline (otherwise P3 
would take the position of its somatic sister C).  During gastrulation 
the two daughters of the primordial germcell P4 follow the E-cells in 
migrating into the center of the egg.  During later embryogenesis the 
two germcells send protrusions into the intestinal cells.  It has been 
speculated that the germcells which have to execute an extensive 
postembryonic program of proliferation may be nursed by the gut cells (
Sulston et al.  ,Dev.  Biol.  100,64-119,1983).  Zur Strassen (
Zoologica 107,1-142,1959) described in detail early development of 
another nematode Bradynema rigidum which differs from the pattern 
found in C.  elegans.  In all early germline divisions the new 
germline cell lies posterior.  Thus, the here discussed reversal of 
division polarity is obviously absent.
Nevertheless, cellular positioning eventually becomes very similar 
to that in C.  elegans because P4 performs a compensating migration 
around its somatic sister D and makes contact to the E-cells.  The 
pattern observed in Bradynema appears simpler and more straightforward.
It may well represent the original pattern which has been modified 
in C.  elegans such that instead of an intercellular reversal of 
polarity an intracellular reversal takes place.  This would abbreviate 
the time needed for embryogenesis and thus would be an evolutionary 
advantage.  How could the reversal of polarity in P2 be controlled?  A 
visible affinity between intestinal precursors and germline cells can 
be observed in untouched embryos of C.  elegans.  In the late 4-cell 
stage the nucleus of P2 is translocated from the posterior region of 
the cell to the anterior-ventral periphery.  After division of EMS and 
P2 the nuclei of E and P3 lie eccentrically side by side separated 
only by the cell membrane.
But if the P2 cell has been extruded in the 4-cell stage, the 
nucleus of E stays in the center of the cell.  Subsequently the cell 
cycle periods in the E-cell lineage are similar (or even identical) to 
those of the MS lineage, in contrast to normal development where the E 
cells express considerably longer cell cycle periods.  Also more than 
the normal 20 E descendants were found in two embryos which were 
analyzed in more detail.  From all this it is concluded that a 
specific cell-cell interaction takes place between P2 and EMS.  This 
interaction appears to be tightly coupled to the reversal of polarity 
described above.  The following working model is suggested: The 
posterior region of the uncleaved egg exerts an attractive force (
induced by sperm entrance?).  This causes the sperm pronucleus to 
remain there while the oocyte pronucleus migrates towards it and 
further causes the P-granules to be prelocalized.  Also in P1 and P2 
nuclei stay therefore most of the cell cycle close to the posterior 
periphery.  After reversal of polarity the attractive force arises 
from the region of P2 adjacent to EMS.  Both blastomeres cleave 
unequally into cells of different developmental potential.  The nuclei 
of E and P3 both react visibly to the attraction with their peripheral 
location.  Herewith the unique behavior of EMS (only somatic sister of 
a germline cell which does not represent a somatic founder cell, but 
passes through an unequal cleavage to generate two of them) finds an