Volume and surface of receptor and auxiliary cells in hygro-/thermoreceptive sensilla of moths (Bombyx mori,Antheraea pernyi,and A. polyphemus)

Summary The thermo/hygroreceptive sensilla styloconica of the silkmoths Bombyx mori, Antheraea pernyi, and A. polyphemus were reconstructed from serial sections of cryofixed and chemically fixed specimens. The volume and surface area of the different sensillar cells were calculated from the area and circumference of consecutive section profiles. In addition, data are provided on the length and diameter of the outer and inner dendritic segments of the receptor cells. The morphometric data obtained from the three species are highly consistent and significantly different from those of olfactory sensilla trichodea of the same species. In each sensillum two type-1 receptor cells (hygroreceptors) are associated with one type-2 cell with a lamellated outer dendritic segment, a comparatively thick inner dendritic segment, and a particularly large soma (thermoreceptor). In contrast to olfactory sensilla, the thecogen cell is the largest auxiliary cell forming an extensive apical labyrinth bordering the inner sensillum-lymph space, whereas an inconspicuous trichogen cell and a medium-sized tormogen cell border a comparatively small outer sensillum-lymph cavity. Moreover, both sensillum-lymph spaces are separated from each other not only by the dendrite sheath, but also by the trichogen cell. The results are discussed with regard to recent electrophysiological observations and current hypotheses on the function of sensilla.     

Ultrastructure of the chemosensitive basiconic single-walled wall-pore sensilla on the antennae in adults and embryonic stages of Locusta migratoria L. (Insecta,Orthoptera)

Summary The structure and embryonic development of the two types (A, B) of basiconic sensilla on the antennae of Locusta migratoria were studied in material that had been cryofixed and freeze-substituted, or chemically fixed and dehydrated. Both types are single-walled wall-pore sensilla. Type-A sensilla comprise 20–30 sensory and 7 enveloping cells. One enveloping cell (thecogen cell secretes the dendrite sheath); four are trichogen cells, projections of which form the trichogen process during the 2nd embryonic molt. The trichogen cells form two concentric pairs proximally. Two tormogen cells secrete the cuticular socket of the sensillum. The dendritic outer segments of the sensory cells are branched. Bifurcate type-A sensilla have also been observed. Type-B sensilla comprise three sensory and four enveloping cells (one thecogen, two trichogen and one tormogen). The trichogen process is formed by the two trichogen cells, each of which gives rise to two projections. The trichogen cells are concentrically arranged. The dendritic outer segments of the sensory cells are unbranched. In the fully developed sensillum, all trichogen and tormogen cells border on the outer receptor lymph cavity. It is suggested that the multicellular organization of the type-A sensilla can be regarded as being advanced rather than primitive.Supported by the Dcutschc Forschungsgemeinschaft (SFB 4/G1)     

Pheromone receptors in Bombyx mori and Antheraea pernyi

Summary The cellular organization of freeze-substituted antennal sensilla trichodea, which contain the sex pheromone receptors, was studied in male silkmoths of two species (Bombyx mori, Bombycidae; Antheraea pernyi, Saturniidae). The cellular architecture of these sensilla is complex, but very similar in both species. A three-dimensional reconstruction of a sensillum trichodeum of B. mori is presented. Two receptor cells (in A. pernyi 1–3) and three auxiliary cells are present. Of the latter, only the thecogen cell forms a true sheath around the receptor cells. A unique thecogen-receptor cell junction extends over the entire area of contact. Septate junctions occur between all sensillar cells apically, and in the region of the axonal origin basally. Gap junctions are also found between all cells except the receptor cells. The trichogen and tormogen cells show many structural indications of secretory activity and are thought to secrete the receptor lymph. Their apical membrane bordering the receptor-lymph space is enlarged by microvilli and microlamellae, but only those of the trichogen cell show regularly arranged membrane particles (portasomes), indicating secretory specialization among the auxiliary cells. Epidermal cells are found as slender pillars between sensilla, but extend apically along the non-sensillar cuticle and basally along the basal lamina.     

Structure of isolated sensilla and sensory neurons in vitro: Observations on developing silkmoth antennae

Summary By combined enzymatic and mechanical treatment, it was possible to dissociate the sensory epithelium of developing antennae of male Antheraea polyphemus and A. pernyi silkmoths from the stage of separation of the antennal branches up to the early stages of cuticle deposition. Large numbers of entire developing trichoid sensilla were isolated. These are characterized by a large trichogen cell with a long apical, hair-forming process and a large nucleus. A cluster of 2–3 sensory neurons, enclosed by the thecogen cell, is situated in the basal region. The dendrites run past the nucleus of the trichogen cell into the apical process from which they protrude laterally. The nuclei of the tormogen and a 4^th enveloping cell can be distinguished near the base of the prospective hair. After further dissociation, only the neuron clusters remain, still enclosed by their thecogen cell and often attached to the antennal branch nerve via their axons. It is finally possible to disrupt the thecogen cells and the axons, leaving the sensory neurons with inner dendritic segments and axon stumps. The majority of these neurons can be expected to be olfactory.     

Immunolocalization of pheromone-binding protein and general odorant-binding protein in olfactory sensilla of the silk moths Antheraea and Bombyx

The distribution of odorant-binding proteins among olfactory sensilla of three moth species was studied by immuno-electron microscopy. Two polyclonal antisera were used in a post-embedding labelling protocol on sections of cryo-substituted antennae. The first was directed against the pheromone-binding protein (PBP) of Antheraea polyphemus, the second against the general odorant-binding protein (GOBP) of the same species. Immunoblots showed that these antisera were highly specific; both antisera did, however, cross-react with related proteins in the related species A. pernyi, and in the bombycid moth B. mori. PBP and GOBP were localized only in olfactory sensilla trichodea and sensilla basiconica, the principal site being the sensillum lymph surrounding the sensory dendrites. In the males of all three species, the pheromone-sensitive long sensilla trichodea exclusively contained PBP. the majority of the sensilla basiconica in both sexes in these species contained GOBP; these sensilla are known to respond to plant and other general odours. Some sensilla were not labelled by either antiserum; presumably, these held an odorantbinding protein of a different subfamily. Never were PBP and GOBP co-localized in the same sensillum. Two observations deserve special attention: (1) PBP was also found in a few sensilla in females, and (2) in B. mori, where the long sensilla trichodea have a different functional specificity in males (pheromone) and females (plant odours), the expression of the odorant-binding protein (males: PBP; females: GOBP) is similarly different. The distinct and complex distribution pattern of odorant-binding proteins supports the notion that these proteins participate in stimulus recognition.Dedicated to Professor Ya.A. Vinnikov on the occasion of his 85. birthdayThis work was partly supported by DFG grant ste 501/3-1.     

Ultrastructure and ontogeny of the hair sensilla on the funicle of Calliphora erythrocephala (Insecta,Diptera)

Summary Four envelope cells are responsible for the formation of the basiconical sensilla of Calliphora. They are the thecogen, trichogen, and tormogen cells, and envelope cell 4. In early stages of development the still subepithelial sensory cilia are completely enclosed by the innermost thecogen cell. The first formation movements are initiated by a growth thrust of the hair-forming cell into the exuvial space. The sensory cilia only begin to grow into the hair anlage when the hair-forming cell has almost reached its final length. As soon as growth is completed the trichogen cell, tormogen cell, and envelope cell 4 start to excrete cuticular material. The trichogen cell forms the perforated part of the hair shaft and the stimulus-conducting system consisting of the pore tubules. The tormogen cell is responsible for the excretion of the basal non-perforated hair shaft and sheath cell 4 forms the proximal part of the socket region. The thecogen cell only begin to produce dendritic sheath material when the sensory hair is almost complete.Approximately 7–8 days after pupation the tormogen cell degenerates, having, by this time, produced about two-thirds of the sensilla cuticle. The surrounding envelope cells incorporate cell fragments of the tormogen cell. The trichogen cell continues the secretion where the tormogen cell left off. When the secretion of cuticle is finished the sheath cells begin to withdraw towards the proximal direction and to form microvilli on the apical membrane. The resulting outer receptor lymph space is bordered by envelope cell 4 and the trichogen and thecogen cells. The tormogen cell is absent in the sensilla of the imago.Abbreviations DS dendritic sheath - E4 envelope cell 4 - Ex exuvial space - G glial cell - iD inner dendritic segment - iRL inner receptor lymph space - oRL outer receptor lymph space - oD outer dendritic segment - P pore - PT pore tubules - S sensory cell - T thecogen cell - TO tormogen cell - TR trichogen cell Part 1 of a dissertation accepted by the Faculty of Bio- and Geosciences, University of Karlsruhe     

The cercal sensilla of the blowfly Lucilia cuprina. II. Structure of the enveloping cells and the basal regions of the sensory dendrites

The gustatory, olfactory, touch and stress receptors on the cerci of Lucilia cuprina Wied. (Diptera: Calliphoridae) have either two or three enveloping cells. The gustatory and olfactory sensilla have three enveloping cells: a tormogen, trichogen and thecogen cell. The tormogen and trichogen cells contribute to a sub-cuticular sensillar lumen which divides into two lobes basally. The thecogen cell forms a lumen around the dendrites. Distally the dendrites lie in the contents of the thecogen lumen within the dendritic sheath. Proximally the dendrites embed in the thecogen cell which has an expanded, microlamellate lumen basally. The sensillar lumen of the mechanosensory (trichoid mechanoreceptors and campaniform) sensilla is formed by a single enveloping cell: the presumptive tormogen cell. In trichoid mechanoreceptors the thecogen lumen is restricted to the region of the transitional region of the dendrite whereas the thecogen lumen of campaniform sensilla extends proximally although it is not as well-developed as that of the chemoreceptive sensilla. The dendrites of all sensillum types on the cerci have a granular body in the transitional region: a situation which has not been previously reported in chemoreceptive sensilla although common in the mechanoreceptors of Calliphoridae and Sarcophagidae.     

Fine structure of the pheromone-sensitive sensilla on the antenna of the hawkmoth, Manduca sexta

The flagellar antenna of the male hawkmoth Manduca sexta carries about 42,000 pheromone-sensitive sensilla trichodea, which are arranged in 'baskets' on the single segments. Each sensillum consists of a cuticular hair up to 500 mum long and is innervated by two bipolar sensory neurons. Each neuron sends an unbranched dendrite into the hair shaft. The dendrite is subdivided by a short ciliary region into an inner and an outer segment. The inner segment is especially rich in smooth vesicles, which accumulate beneath the ciliary region where they seem to fuse with the dendritic membrane. The outer dendritic segment often shows conspicuous 'beads' along its length. Three auxiliary, or enveloping, cells belong to each adult sensillum. These are the thecogen, the trichogen, and the 'outer' cell. Most probably, the latter is not homologous with the 'traditional' tormogen cell from a genealogical point of view.     

Are Odorant-binding Proteins Involved in Odorant Discrimination?

Pheromone-sensitive sensilla trichodea of nine moth speciesbelonging to six families and three superfamilies of Lepidopterawere immunolabelled with an antiserum against the pheromone-bindingprotein of Antheraea polyphemus. Strong immunolabelling of thesensillum lymph was observed in all long sensilla trichodeaof A. polyphemus, A. pernyi (Saturniidae), Bombyx mori (Bombycidae)and Manduca sexta (Sphingidae). Very weak labelling was foundwith all sensilla trichodea of Dendrolimus kikuchii (Lasiocampidae)and Lymantria dispar (Lymantriidae). In three noctuid species,some long sensilla trichodea were labelled strongly, some onlyweakly and some were not labelled at all. The fraction of longsensilla trichodea that were strongly labelled was large inHelicoverpa armigera, but small in Spodoptera littoralis andAutographa gamma. The observed cross-reactivity was not correlatedwith taxonomic relatedness of the species but rather with chemicalrelatedness of the pheromones used by these species, as a highlabelling density was consistently observed in sensilla tunedto pheromones with an alcyl chain of 16 carbon atoms. The highlydivergent specificity of pheromone-receptor cells in Noctuidaeappears to be mirrored by a similar diversity of the pheromone-bindingproteins in the sensilla trichodea. These data support the notionthat pheromone-binding proteins participate in odorant discrimination.Chem. Senses 21: 719–727, 1996.     

Cellular organization of the dome sensillum: A presumed chemoreceptor in Gammarus setosus (Gammaridea: Amphipoda)

A previously unknown type of sensillum with a thin cuticular dome and two pairs of pores is described in the amphipod Gammarus setosus. There is only one dome sensillum on each interantennal lobe of the head. The receptor is innervated by two sensory dendrites that bifurcate into two pairs of 9 + 0 cilia, concentrically enclosed by four auxiliary cells—two thecogen, one trichogen, and one tormogen and surrounded by a cluster of accessory cells. The ciliary regions are contained in small inner lymph cavities. The outer segments are sheathed by the apical extensions of the thecogen cells, are looped inside the outer lymph cavity, and come in close contact with lipid spheroids inside the dome. The basal bodies consist of microtubule doublets, which extend into the distal segments where they are interspersed with singlets. The nodal inner dendritic segments join the ventral suspension cord of the organ of Bellonci and enter its ganglion. The application of colloidal lanthanum resulted in intraciliary lanthanum deposits. The dome sensilla are presumed to be chemosensory because their cellular plan has similarities to that of some known olfactory and pheromone-sensitive sensilla in decapod crustaceans and insects. © 1994 Wiley-Liss, Inc.