Epithelial System of the Male (Part II) - Sensilla: The Rays

Ray composition and structure -Ray development -Ray Identity -Ray neuron connectivity -Acknowledgements - Back to Contents

Ray composition and structure

Nine bilateral pairs of finger-like rays (numbered (n) 1 to 9, Left/Right) radiate from the tail and are embedded in a cuticlar fan (MaleEpiFIG11A). In male mating behavior the rays are required for initial contact reponse upon encountering the hermaphrodite and for turning during the male's search for the vulva (MaleEpiFIG10C - MALE EPITHELIAL SYSTEM - Part II: Overview; Liu and Sternberg, 1995; reviewed in WormBook: Male Mating Behavior - Barr and Garcia).

All rays have the same cellular composition and general organization (MaleEpiFIG11B). Each contains sensory dendrites of an A-type (RnA) and B-type (RnB) neuron (MaleEpiTABLE1A). Neuron processes are surrounded by a tube formed by the ray's single interfacial cell, the ray structural cell (Rnst) (MaleEpiFIG12A-C; Sulston and Horvitz, 1977; Sulston et al., 1980). The Rnst, in turn, is ensheathed by hyp7 and by cuticle. Except for ray 6, all rays are open at their tip. This opening is visible by DIC optics as a "ring-and-dot" formed by the hyp and Rnst encircling the RnB tip (MaleEpiFIG11B, 13E). Despite being exposed to the environment, RnB neurons do not dye-fill with FITC or Di0 (Perkins et al., 1986). The RnA, RnB and Rnst cells of a single ray are closely related by lineage, arising from a common great-grandmother precursor cell, Rn (MaleEpiFIG11C)

MaleEpiTABLE1A: Summary of Ray Cells

Cell type

Cell name Lineage name Syncytial No. nuclei Other noteworthy features
Structural cell RnstL/R

Rn.appL/R

no 1 functions as both sheath and socket cell
Sensory or sensory-motor neuron RnAL/R

Rn.aaaL/R

no 1 striated rootlet, ends within ray
Sensory neuron RnBL/R

Rn.apaL/R

no 1 Except for R6BL/R: A large cell body containing dilated cisternae. A tip surrounded by a cylinder of cuticle. Dendrite contains a transition zone and tip is exposed to environment.
n stands for rays 1-9. Rn = V5/V6 /T.xxxxx in the male. R1 derives from V5, R2-6 from V6 and R7-9 from T.

 

Ray cells of each side are located together in their respective left or right lumbar gangila (LGL/R) (MaleEpiFIG11C,D). Cell body positions within the gangila are variable. Except for R6BL/R, RnB neurons have large cell bodies that contain dilated cisternae (MaleEpiFIG11E). Ray neurons (but not the Rnsts) send axons, via commissures, from the LGL/R to the pre-anal ganglion (PAG) (MaleEpiFIG11C;MaleEpiFIG12A-C; Sulston et al., 1980).

The Rnst cell functions both as a sheath and a socket cell. Like the sheath cell, the Rnst surrounds neuron dendrites and contains numerous vesicles that presumably secrete material into the ray lumen. Like the socket cell, the Rnst acts as a transitional cell linking the sense organ to the surrounding hyp via adherens junctions (MaleEpiFIG13A-C).

 

Ray development

Rays are generated post-embryonically from the most posterior L1 lateral seam cells of each side, V5 (L/R), V6 (L/R) and T (L/R) (see EPITHELIAL SYSTEM OF THE MALE -PART I ). The characteristic finger-like structure of the ray is generated by a process of morphogenesis whereby part of each ray cell remains attached to the body wall while surrounding hyp and body wall tissues migrate anteriorly (summarized in MaleEpiFIG13E; see EPITHELIAL SYSTEM OF THE MALE -PART I for details). Interactions between the Rnst and hyp are thought to play an important role in ray morphogenesis. Loss of function mutations in several genes cause a lumpy ray phenotype or disrupt ray extension (a Ram phenotype - ray abnormal morphology or a Mab phenotype - male abnormal). Characterization of one such gene, ram-5, reveals that it encodes a novel protein that is expressed in the Rnst cells and may act in a glycosylation-dependent pathway that regulates hyp and Rnst cell-cell interactions (Yu et al., 2000; Ko and Chow, 2003).

 

Ray identity

The Rnst is also thought to play a role in defining ray-specific morphology. Each left/right ray pair has a characteristic shape and opens on a particular side of the fan (MaleEpiFIG11A; MaleEpiTABLE1B). These morphological attributes, expressed along with distinct combinations with neuronal characteristics (e.g. neurotransmitter fate, axons trajectory, chemosensory receptor), give each ray pair a unique identity (Sulston and Horvitz, 1977; Loer and Kenyon, 1993; Troemel et al., 1995; Lints et al., 2004; L. Jia and S.W. Emmons, pers. com.). Ray identities may reflect functional specialization of rays in aspects of mating behavior. For example, dorsally-opening rays (rays 1, 5, and 7) are required for contact response during a dorsal encounter with a hermaphrodite; ventrally-opening rays (rays 2, 4, and 8) function with other ventral sense organs in ventral encounters; the posterior T rays (7-9) are required for turning (Liu and Sternberg, 1995). Ray identities are specified by regulators (including Hox genes, a TGF-beta signal, DM-domain and Pax-6 transcription factors) that act in distinct combinations in each ray pair (Chow and Emmons, 1994; Savage et al. 1996, Zhang and Emmons, 1995; Lints and Emmons, 1999; Lints and Emmons, 2002; reviewed in WormBook: Male Development - Emmons).

MaleEpiTABLE1B: Summary of Ray Identity Characteristics

Ray

Morphology* Opening* Dilated cisternae in RnB cell body
PKD-2, LOV-1, CWPs -positive RnB neuron
RnA transmitters

RnB transmitters

1 thin

dorsal

yes
yes
flp-5, flp-17
2 thick, short

ventral

yes
yes
FLP anti-sera-positive, flp-6
3 thin, extends to margin

margin

yes
yes
5HT
4 thin ventral yes
yes
5 thin dorsal yes
yes
DA
flp-5, flp-6, flp-17
6 thick, tapered, ends short of the margin none no
no
flp-6
7 thin dorsal yes
yes
DA
flp-5, flp-6, flp-17
8 thin ventral yes
yes
9 thin, extends to margin margin yes
yes
DA
5HT

* may be defined by differentiated characteristics the Rnst cell. PKD-2 / LOV-1 expression: Barr and Sternberg, 1999. CWP-1, -2, -3 and -4: Portman and Emmons, 2004. DA (dopamine): Sulston and Horvitz, 1977. 5HT (serotonin): Loer and Kenyon, 1993, Lints et al., 2004. flp/FLP (FMRFamide-like-peptide reporters for flp-5, flp-6, flp-17 /antibody-positive): Lints et al., 2004.

Ray neuron connectivity

Early reconstruction data suggest that neurons of different rays may synapse with different combinations of targets (The Male Wiring Project). The data also suggest that there may be a high degree of connectivity between neurons of certain rays (MaleEpiFIG13F; see R3B INDIVIDUAL NEURON PAGE). As observed in the post-cloacal sensilla, some rays (e.g. R3AL) may be motor as well as sensory neurons because they form neuromuscular junctions with sex muscles (MaleEpiFIG13G; MALE MUSCLE SYSTEM -Part I: Longitudinal Muscles).

Acknowledgements

We would like to thank Douglas Portman (University of Rochester, NY) for critically reviewing this chapter for us.

 


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