The Seam - The tail tip hyp - Cell list - Acknowledgements - Back to Contents
In the male, the three most posterior L1 lateral seam cells, V5 (L/R) , V6 (L/R) and T (L/R), produce the sensory rays, instead of alae-secreting seam cells (MaleEpiFIG2A). Rays are required for various steps in male mating behavior (to view behavior see MALE HANDBOOK-INTRODUCTION, Part 1).
The adult male tail bears a total of nine bilateral pairs of rays (numbered, n, 1 to 9 from anterior to posterior, Left/Right) which are embedded in a cuticular fan (MaleEpiFIG2B). Each ray consists of the dendritic endings of two sensory neurons (an RnA and an RnB neuron), surrounded by an epithelial tube formed by a ray structural cell (Rnst). All ray cell processes are ensheathed in an extension of hyp7 and cuticle (MaleEpiFIG2B; for details see MALE HANDBOOK-EPITHELIAL SYSTEM OF THE MALE-Part II). Except for ray 6, the tips of the rays open to the environment. At light microscope resolution ray openings can be seen as a "ring-and-dot", formed by the hyp and Rnst cell encircling the RnB neuron tip. Ray development spans L2 to late L4 and can be divided into two non-overlapping phases (1) ray cell generation and (2) ray morphogenesis.
1. Ray cell generation
The first signs of sexual dimorphism in the seam are apparent at L2 where male V5 and V6 lineages execute a doubling division and the T lineage divides (MaleEpiFIG3A). The daughters of the V5 and V6 doubling division, and T, divide to produce 9 ray precursor (Rn) cells in each seam by L3 (MaleEpiFIG3C, top row).
Between mid-L3 and mid-L4, each Rn cell divides by a stereotyped lineage pattern (referred to as the ray sublineage) producing the constituent cells of a single ray: an RnA, RnB and Rnst cell (a Ray Cell Group, RCG) (MaleEpiFIG3B, 3C). Thus, the cells of a single ray derive from a common precuror. Execution of the sublineage is driven by members of the conserved basic-helix-loop-helix proneural gene family (LIN-32 and HLH-2; Zhao and Emmons, 1995; Portman and Emmons, 2000) and a DM domain gene (MAB-3; Yi et al. 2000; Ross et al, 2005). In addition to a RCG, each Rn produces 1 hypodermal cell (Rn.p) that will either fuse with Rn.p cells from other rays forming the male posterior seam (SET) cell (R1.p-R5.p) or will fuse with hyp 7 (R6.p-R9.p; Sulston et al., 1980).
2. Ray Morphogenesis
After completion of the ray sublineages the hypodermis, ray cell bodies and other cells of the posterior migrate anteriorly as part of the process of reshaping the male tail. Ray cell bodies detach from the body wall and migrate anteriorly and medially to the lumbar ganglia (LG L/ R) (MaleEpiFIG4B, 6D). A small part of each ray cell, however, remains attached to the body wall and the general forward movement of hyp and ray cell bodies spins out the rays (MaleEpiFIG5B, 5C).
Nascent rays initially appear as papillae on the surface of the tail (MaleEpiFIG5A-C) and subsequently lengthen as surrounding tissues continue to move forward. The fan forms from cuticle that separates from the body wall at the lateral sides of the animal (MaleEpiFIG4B). The gap formed is bridged by the developing rays. The inner layer of the adult cuticle is laid down and the lateral portions of cuticle collapse around the rays forming the fan. The ray tips characteristically open on either the dorsal (rays 1, 5 and 7) or ventral (rays 2, 4 and 8) fan surface or at the fan margin (rays 3 and 9) (Sulston et al., 1980) and this is established when the ray papillae initially attach to the cuticle (as shown in MaleEpiFIG5B, 5C).
As mentioned above, a small part of each ray cell is connected to the body wall and these fixed points of attachment, coupled with retraction of surrounding tissues, drive ray formation. Ultrastructurally the attachments consist of adherens junctions (AJs) interlinking hyp, Rnst and ray neurons as well as hemidesmosomes (HDs), that link hyp to cuticle (MaleEpiFIG6A-C).
During the course of ray cell generation and morphogenesis some cell-cell contacts are maintained while others change (Baird et al., 1991). For example, the constituent cells of the RCG remain in tight association throughout ray development and do not intermingle with cells of other rays (MaleEpiFIG4A). This is reminiscent of the phenomenon of lineage restriction, observed in the Drosophila imaginal disc compartments or in the rhombomeres of vertebrate hindbrain. By contrast, RCGs must separate from the SET in order for future rays adopt their adult axial positions. Cell affinities and migrations are regulated by conserved cell attraction and repulsion factors such as ephrins, semaphorins and plexins (Roy et al, 2000; Ginzburg et al, 200; Hahn and Emmons, 2003; Dalpe et al, 2004). Mutations in genes encoding such factors cause abnormal ray positioning or fusion of rays (for EM analysis of fused ray ultrastructure see Chow et al., 1995).
During late L4 the male tail tip changes from a tapering cone shape (leptoderan) to a blunt dome (peloderan) (MaleEpiFIG1A; for animation visit Fitch lab website). Tail tip remodeling is the first step in establishing the adult male posterior form. Prior to tip morphogenesis, male and hermaphrodite tail tips differ only slightly in their cell contacts and composition (MaleEpiFIG7). In both sexes the tip contains the 4 hyp cells hyp8-11. In males, however, the sisters of T form a binucleate cell called hyp13, instead of fusing with hyp7 as in the hermaphrodites (Sulston et al., 1983). Cell contacts are largely the same except that in males hyp11 borders with male-specific ray lineage cells and hyp8 with hyp13. The distribution and frequency of adheren junctions (AJs) and gap junctions (GPs) between tail tip cells does not differ significantly between the sexes at this stage (Nguyen et al., 1999).
Tail tip remodelling occurs at the same time as ray morphogenesis (begining mid L4, ca 35 hrs; MaleEpiFIG8). The process can be divided into approximately 5 stages (Sulston et al., 1980; Nguyen et al., 1999). Cell borders break down (visualized by the disappearance of adherens junction marker AJM-1::GFP/MH27 antibody staining) and cells fuse together (Stages 0-2). Fusion progresses from the anterior to posterior of the tail tip. EM analysis of fusing cells suggest that fusions initiate at or near adherens junctions (Nguyen et al., 1999).
The newly formed tail tip syncytium then migrates anteriorly into the body at the midline until it forms a strip of central hyp that extends from the tail to the anterior edge of the proctodeum (Stages 3-5 and adult in MaleEpiFIG9A, 9B).
All contents are copyright ©2002-2005 Wormatlas unless otherwise noted. See copyright and use policy.