Worm Breeder's Gazette 9(3): 106

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.

Morphogenesis of the Male Tail

S. Emmons

During a sabbatical year at the MRC Laboratory in Cambridge, England,
I isolated mutants that affect formation of the copulatory structures 
of the adult male tail (mab), and studied the process of tail 
morphogenesis.
The most obvious feature of the adult male tail is the cuticular fan 
with its nine rays. This structure, consisting of a large fold in the 
outer layer of the cuticle, is formed when the cells that inhabit the 
posterior region of the L4 larva retract just before the L4/adult molt 
(Sulston et al., Dev. Biol. 78, 542-576 (1980)). As the cells withdraw 
anteriorly, the outer layer of the newly-formed adult cuticle is left 
behind and eventually folds in a precise way to form the fan. Two 
questions arise concerning this process: what is the mechanism of cell 
withdrawal, and how is the cuticular folding accomplished in such a 
precise way, with reproducible and sharp boundaries?
It can be seen, by comparison of the volume of the animal before ar_ 
after withdrawal of the posterior cells, that retraction must be 
accompanied by extrusion of a large amount of fluid from the body. 
This fluid passes into the growing space between the retreating cells 
and the L4 cuticle, and is under pressure. In order to see whether the 
pressure affected the morphogenetic movements, a hole was made in the 
L4 cuticle with the laser microbeam during the morphogenetic process. 
When the cuticle was punctured, the fluid escaped in a rush, and 
morphogenesis stopped. The partially retracted cells bulged back 
against the L4 cuticle. This result could mean that retraction of the 
posterior cells is driven by pressure between the L4 and adult 
cuticles. Alternatively, it might simply mean that the newly-forming 
adult cuticle is not yet strong enough to resist internal body 
pressure. To test this idea worms were observed in hypertonic medium (
e.g., 6% glucose), where pressure is reduced in both the space in the 
tail between the L4 and adult cuticles, and in the body generally, 
because of loss of water through the cuticle. In hypertonic medium, 
morphogenesis of the tail is also arrested. This result makes it 
appear that liquid pressure in the space between the adult and L4 
cuticles is necessary per se for the morphogenetic movement. This 
pressure would act along with retraction caused by muscles in the tail,
and possibly other cellular mechanisms, to mold the final shape of 
the adult body.
As retraction proceeds, folding of the fan occurs against the taut 
L4 cuticle, which may act as a sort of scaffold or mold for the 
process. This may help to explain the preciseness of the shape of the 
fan, but it cannot account for its boundaries. Retraction of the body 
occurs well beyond the boundaries of the fan. Beyond the fan the inner 
and outer layers of the adult cuticle no longer separate. Instead, the 
outer cuticular layer adheres to the inner layer and the surface of 
the body. The outer cuticular layer and its behavior can be observed 
under Nomarski optics during the morphogenetic process. A critical 
aspect of fan formation must involve synthesis of a special type of 
cuticle, in which inner and outer layers are not joined, over the 
surface where the fan will eventually form during retraction.
Electron micrographs of serial sections of males in the late L4 
stage were examined to determine what cells might be responsible 
for
making this special cuticle. The electron micrographs were made by 
Sulston and coworkers in their earlier studies of the male. Much of 
the tale hypodermis in the late L4 larva is made up from the posterior 
daughters of the ray precursor cells, Rn (n=1-9), which come to lie 
roughly underneath the region where the outer cuticular layer will 
separate to form the fan. Further analysis of electron micrographs, 
along with laser ablation experiments, are necessary to determine 
whether these and possibly other hypodermal cells are indeed 
responsible for making the fan.
In genetic studies, nine new mab mutations were isolated by 
screening males in clones of a mutagenized him strain for 
abnormalities. One mutation is a new allele of the previously-
identified gene mab-11, and the others are probably in new mab genes. 
Abnormalities affect various structures, from the spicules to the fan 
and rays, and ranged from subtle to severe.
One severe mutant was examined in more detail, and surprisingly was 
found to undergo a nearly normal morphogenetic process, up until the 
time that the L4 cuticle was breached in molting. At this point, the 
normally-shaped tail bulged back out and spoiled the nearly-normal fan,
in somewhat the same manner as occurred when the L4 cuticle was 
prematurely punctured with the laser. This gene therefore appears to 
encode a product required to hold the definitive fan in place. The 
same mutant is ts for alae formation in the adults of both sexes, and 
has severe cuticle defects in the L1 larva, which is osmotically 
sensitive. Therefore the protein may also be used to maintain alae (
present exclusively in L1's, dauers, and adults - dauers were not 
examined in these experiments). Alae, like the fan, consist of a 
cuticular fold, and are formed by seam cells. (The ray precursor cells,
Rn, are descended from seam cells.) We propose that this mutation 
affects a cuticle component required to maintain the structure of both 
alae and fan, and may identify a component of a morphogenetic 
'subprogram' used in making these two structures.