Morphology and ultrastructure of pharyngeal sense organs of Drosophila larvae
- Department of Genetics, University of Leipzig, Institute for Biology, Germany
- MRC Laboratory of Molecular Biology, Cambridge Biomedical Campus, United Kingdom
- Department of Physiology, Development and Neuroscience, University of Cambridge, United Kingdom
- German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Germany
Figures
Figure 1
Localization and analysis of the cellular configuration of the larval pharyngeal sensilla.
(A) Depiction of the workflow for identification of larval pharyngeal sense organs and sensilla types. A previously generated scanning transmission EM (STEM) volume of a whole first instar D. melanogaster larva (Peale et al., 2024) was used to localize all cells associated with the larval sensilla using CATMAID (Saalfeld et al., 2009). Smaller volumes were extracted from this volume to generate single organ or sensillum 3D volumes. These volumes were analyzed and manually reconstructed to describe and classify the types of pharyngeal sensilla and their corresponding sensory neurons. (B) Schematic drawing of the main external and pharyngeal organs of the larval head region. The projections via the main nerves into the subesophageal zone (SEZ) are visualized. Sensilla and sensory neurons were reconstructed from their distal ends to their ganglia. Axonal projections were not reconstructed. The numbers in the circles indicate the number of neurons in the respective ganglion. The pharynx (ocher), brain (gray), main external head organs, and pharyngeal organs are highlighted. These organs are the dorsal organ (DO; purple), the terminal organ (TO; blue), the ventral organ (VO; light blue), the labial organ (LO; turquoise), the dorsal pharyngeal sensilla (DPS; yellow), the dorsal pharyngeal organ (DPO; orange); ventral pharyngeal sensilla (VPS; bright green); and posterior pharyngeal sensilla (PPS; red). Abbreviations: D – dorsal; V – ventral; A – anterior; P – posterior; L1 – first instar; CB – central brain; SEZ – subesophageal zone; VNC – ventral nerve cord; AN – antennal nerve; MxN – maxillary nerve; LrN – labral nerve; LbN – labial nerve; CPS – cephalopharyngeal skeleton; DOG – dorsal organ ganglion; TOG - terminal organ ganglion; VOG – ventral organ ganglion; LOG – labial organ ganglion; DPSG – dorsal pharyngeal sensilla ganglion; DPOG – the dorsal pharyngeal organ ganglion; VPSG – ventral pharyngeal sensilla ganglion; PPSG – posterior pharyngeal sensilla ganglion.
Figure 2 with 5 supplements
Main cellular configuration of the ventral pharyngeal sensilla (VPS).
(A) 3D reconstruction of the sensory neurons innervating the VPS. The VPS is a bilaterally organized organ, but the left and right sides are fused. Only the reconstructions of the five sensilla on the left are shown. These are two papillum sensilla (P1 and P2), a modified papillum sensillum (Pmod), a hair-like sensillum (H1), and a pit sensillum (T1). Ultrastructural features of the outer and inner morphology were used to classify the different sensilla. These sensilla resemble canonical sensilla types that can also be found in the terminal organ (see Figure 1A), the main external gustatory organ. They display different features like a terminal pore (pit sensillum – T) or a sensillum shaft (modified papillum sensillum – Pmod; hair-like sensillum – H), or both (papillum sensillum – P). Mechanosensory cells are identified by their inner dendritic morphology, which contains a tubular body, a structure known to be important for mechanosensation. For a detailed description of the single VPS sensilla, see Figure 2—figure supplements 1–5. Nomenclature for sensilla was adapted from previous work (Chu-Wang and Axtell, 1972; Rist and Thum, 2017). The number of neurons innervating the sensilla is indicated in brackets. (B) STEM section of the VPS showing the organ’s midline (dashed line). The sensilla of the right side are highlighted, and the innervating neurons are color-coded for their putative sensory function (purple – gustatory; green – mechanosensory). (C) 3D reconstruction of the outer morphology of the VPS. The position of the sensilla is indicated for the right side of the fused organ. Unlike the other pharyngeal sensilla (see Figures 3 and 4), the VPS display prominent outer structures that extend into the pharyngeal cavity. Abbreviations: d – dorsal; v – ventral; a – anterior; p – posterior; P – papillum sensillum; Pmod –modified papillum sensillum; H – hair sensillum; T – pit sensillum. Scale bars: B: 1 µm.
Figure 2—figure supplement 1
VPS-P1.
Internal morphology of the papillum sensillum 1 (P1) of the ventral pharyngeal sensilla (VPS). (A) 3D reconstruction of the sensory neurons innervating the P1 sensillum. Three sensory neurons innervate P1. (B) 3D reconstruction of the outer morphology of the VPS. The arrow indicates the location of the P1 sensillum. (C–I) Serial scanning transmission electron microscopy (STEM) sections of the P1 sensillum. (C, D) The sensillum shaft is visible. The terminal pore is innervated by sensory neurons (purple). (E) Further proximal, all three cilia are visible. Two neurons (purple) are innervating the terminal pore, and one neuron (turquoise) ends at the base of the pore with a tubular body. A dendritic sheath is present. (F) The three dendrites are bathed in the sensillum lymph and enclosed by the dendritic sheath. The thecogen, trichogen, and tormogen support cells are highlighted. (G) The three dendrites are bathed in the sensillum lymph, but the dendritic sheath is absent at this level. (H) The sheath cell is highly compartmented and lamellated at this level. (I) Section of the VPS ganglion. The cell bodies of the three P1 neurons are visible. Abbreviations: po – pore; sh – shaft; ct – cuticle tube; ds – dendritic sheath; tb – tubular body; sl – sensillum lymph; lm – lamellae. Scale bars: C–H: 1 µm; I: 5 µm.
Figure 2—figure supplement 2
VPS-P2.
Internal morphology of the papillum sensillum 2 (P2) of the ventral pharyngeal sensilla (VPS). (A) 3D reconstruction of the sensory neurons innervating the P2 sensillum. Three sensory neurons innervate P2. (B) 3D reconstruction of the outer morphology of the VPS. The arrow indicates the location of the P2 sensillum. (C–I) Serial scanning transmission electron microscopy (STEM) sections of the P2 sensillum. (C, D) The sensillum shaft is visible. The terminal pore is innervated by sensory neurons (purple). (E) Further proximal, all three cilia are visible. Two neurons (purple) are innervating the terminal pore, and one neuron (turquoise) ends at the base of the pore with a tubular body. A dendritic sheath is present. (F) The three dendrites are bathed in the sensillum lymph and enclosed by the dendritic sheath. The thecogen, trichogen, and tormogen support cells are highlighted. (G) The three dendrites are bathed in the sensillum lymph, but the dendritic sheath is absent at this level. (H) The sheath cell is highly compartmented and lamellated at this level. (I) Section of the VPS ganglion. The cell bodies of the three P2 neurons are visible. Abbreviations: po – pore; sh - shaft; ct – cuticle tube; ds – dendritic sheath; tb – tubular body; sl – sensillum lymph; lm – lamellae; gl – ganglion. Scale bars: C–H: 1 µm; I: 5 µm.
Figure 2—figure supplement 3
VPS-Pmod.
Internal morphology of the modified papillum sensillum (Pmod) of the ventral pharyngeal sensilla (VPS). (A) 3D reconstruction of the Pmod sensillum. A single sensory neuron innervates Pmod. (B) 3D reconstruction of the outer morphology of the VPS. The arrow indicates the location of the Pmod sensillum. (C–I) Serial scanning transmission electron microscopy (STEM) sections of the Pmod sensillum. (C, D) The sensillum shaft is visible. Its shaft forms a cylindrical portion that encircles a bud-like structure. The bud lacks a terminal pore. (E) Further proximal, the neuron (turquoise) at the base of the shaft is visible. The neuron ends with a tubular body. A dendritic sheath is present. (F) The dendrite is entirely enclosed by the dendritic sheath. The thecogen, trichogen, and tormogen support cells are highlighted. (G, H) The dendrite is bathed in the sensillum lymph, but the dendritic sheath is absent at this level. The sheath cell is not compartmented and lamellated. (I) Section of the VPS ganglion (VPSG). The cell body of the Pmod neuron is visible. Additionally, three cell bodies of multidendritic sensory neurons (Type II neurons) lie in the VPSG (two cell bodies and one dendrite visible in this section). A heterodynal chordotonal organ lies close to the VPSG. Abbreviations: sh – shaft; tb – tubular body; ds – dendritic sheath; sl – sensillum lymph; gl – ganglion; MDN – multidendritic neuron; ChO – chordotonal organ. Scale bars: C–H: 1 µm; I: 5 µm.
Figure 2—figure supplement 4
VPS-H1.
Internal morphology of the hair-like sensillum 1 (H1) of the ventral pharyngeal sensilla (VPS). (A) 3D reconstruction of the H1 sensillum. A single sensory neuron innervates H1. (B) 3D reconstruction of the outer morphology of the VPS. The arrow indicates the location of the H1 sensillum. (C–I) Serial scanning transmission electron microscopy (STEM) sections of the H1 sensillum. (C, D) The sensillum shaft is visible. Its shaft forms a hair-like structure. The hair lacks a terminal pore. Externally, the shaft is hardly visible as the other prominent VPS sensilla mask it. (D, E) The neuron (turquoise) at the base of the shaft is visible. The neuron ends with a tubular body. A dendritic sheath is present. (F) The dendrite is entirely enclosed by the dendritic sheath. (G) The dendrite is bathed in the sensillum lymph, but the dendritic sheath is absent at this level. The thecogen, trichogen, and tormogen support cells are highlighted. (H) The sheath cell is not compartmented and lamellated. (I) Section of the VPS ganglion. The cell body of the H1 neuron is visible. Abbreviations: sh – shaft; ds – dendritic sheath; tb – tubular body; sl – sensillum lymph; ids – inner dendritic segment; gl – ganglion. Scale bars: C–H: 1 µm; I: 5 µm.
Figure 2—figure supplement 5
VPS-T1.
Internal morphology of the pit sensillum 1 (T1) of the ventral pharyngeal sensilla (VPS). (A) 3D reconstruction of the T1 sensillum. Two sensory neurons innervate T1. (B) 3D reconstruction of the outer morphology of the VPS. The arrow indicates the location of the T1 sensillum. (C–I) Serial scanning transmission electron microscopy (STEM) sections of the T1 sensillum. (C) The terminal pore is visible. A cuticle tube connects to the lumen through a pore and is innervated by the dendrites. (D) The cuticle tube connects with the dendritic sheath. (E) The two ciliary structures (purple) are visible. A dendritic sheath is present. The trichogen and tormogen support cells are highlighted. (F) The tips of the dendrites are enclosed by the dendritic sheath, and the proximal parts are bathed in the sensillum lymph enclosed by the sheath cell. The thecogen and trichogen support cells are highlighted. (G) The dendrite is bathed in the sensillum lymph, but the dendritic sheath is absent at this level. The sheath cell is lamellated. (H) Inner dendritic segment of one sensory cell (I) Section of the VPS ganglion. The cell bodies of the T1 neurons are visible. Abbreviations: po – pore; ct – cuticle tube; ds – dendritic sheath; sl – sensillum lymph; lm – lamellae; ids – inner dendritic segment; gl – ganglion. Scale bars: C–H: 1 µm; I: 5 µm.
Figure 3 with 7 supplements
Main cellular configuration of the dorsal pharyngeal sensilla (DPS).
(A) 3D reconstruction of the sensory neurons innervating the DPS. The DPS is a bilaterally organized organ; only the reconstructions of the seven sensilla on the left are shown. These are two papilla/spot sensilla (P/S1 and P/S2) and five pit sensilla (T1 – T5). From the ganglion, the sensilla expand to an anterior and a posterior location. In the anterior group, we find three pit sensilla (T1, T2, and T3) and two papilla/spot sensilla (P/S1 and P/S2), the latter of which is located in a deep channel. The pit sensilla display an idiosyncrasy as they share their terminal pore into the pharyngeal lumen. The posterior group consists of two pit sensilla (T4 and T5), which share a terminal pore, too. Ultrastructural features of the outer and inner morphology were used to classify the sensilla. For a detailed description of the single DPS sensilla, see Figure 3—figure supplements 1–7. The nomenclature for sensilla was adapted from previous work (Chu-Wang and Axtell, 1972; Rist and Thum, 2017). The number of neurons innervating the sensilla is indicated in brackets. (B, C) Scanning transmission electron microscopy (STEM) section of the anterior group (B) and posterior group (C) of the DPS. The sensory neurons innervating the sensilla are highlighted and color-coded for their putative sensory function (purple – gustatory; green – mechanosensory). Abbreviations: d – dorsal; v – ventral; a – anterior, p – posterior; P/S – papilla/spot sensillum; T – pit sensillum. Scale bars: B: 1 µm; C: 1 µm.
Figure 3—figure supplement 1
DPS-P/S1.
Internal morphology of the papilla/spot sensillum 1 (P/S1) of the dorsal pharyngeal sensilla (DPS). (A) 3D reconstruction of the P/S1 sensillum. A single sensory neuron (turquoise) innervates P/S1. (B–G) Serial scanning transmission electron microscopy (STEM) sections of the P/S1 sensillum. (B) The P/S1 sensillum sits at the anterior end of the pharyngeal cavity (ph). (C) Its dendrite exhibits a tubular body at the tip. A dendritic sheath is present. The sensillum lacks a terminal pore. (D) Further proximal, the dendrite tapers down and thickens again (E). The dendrite is entirely enclosed by the dendritic sheath. (F) The dendrite is bathed in the sensillum lymph, but the dendritic sheath is absent at this level. The thecogen, trichogen, and tormogen support cells are highlighted. (G) Section of the VPS ganglion. The cell body of the P/S1 neuron is visible but lies beside the ganglion. Abbreviations: ds – dendritic sheath; tb – tubular body; sl – sensillum lymph; gl – ganglion. Scale bars: B–G: 1 µm.
Figure 3—figure supplement 2
DPS-P/S2.
Internal morphology of the papilla/spot sensillum 2 (P/S2) of the dorsal pharyngeal sensilla (DPS). (A) 3D reconstruction of the P/S2 sensillum. A single sensory neuron (turquoise) innervates S2. (B–G) Serial scanning transmission electron microscopy (STEM) sections of the P/S2 sensillum. (B) The P/S2 sensillum sits at the anterior end of the pharyngeal cavity (ph) in a deep ‘cuticle’ channel (2,5 µm). (C) Its dendrite exhibits a tubular body at the tip. A dendritic sheath is present. The sensillum lacks a terminal pore. (D) Further proximal, the dendrite thickens (E). The dendritic sheath entirely encloses the dendrite. (F) The dendrite is bathed in the sensillum lymph, but the dendritic sheath is absent at this level. The thecogen, trichogen, and tormogen support cells are highlighted. (G) Section of the VPS ganglion. The cell body of the P/S2 neuron is visible and lies inside the ganglion. Abbreviations: ds – dendritic sheath; tb – tubular body; sl – sensillum lymph; gl – ganglion. Scale bars: B–G: 1 µm.
Figure 3—figure supplement 3
DPS-T1.
Internal morphology of the pit sensillum 1 (T1) of the dorsal pharyngeal sensilla (DPS). (A) 3D reconstruction of the T1 sensillum. Two sensory neurons (purple) innervate T1. The sensillum shares a terminal pore to the pharyngeal lumen with pit sensilla T2 and T3 (see Figure 3—figure supplements 4 and 5). (B–G) Serial scanning transmission electron microscopy (STEM) sections of the T1 sensillum. (B) The T1 sensillum sits in a small pore at the anterior end of the pharyngeal cavity. (C) Its dendrites extend into the pore through the cuticle tube, together with the T2 and T3 dendrites. (D) Further proximal, the dendritic sheaths separate the dendrites of T1 – T3 from each other. (E) The dendrites’ ciliary structures are visible and entirely enclosed by the dendritic sheath(s). The trichogen and tormogen support cells are visible. (F) The dendrites are bathed in the sensillum lymph, but the dendritic sheath disintegrates at this level. The thecogen, trichogen, and tormogen support cells are visible. (G) Section of the VPS ganglion. The cell bodies of the T1 neurons are visible and lie inside the ganglion. Abbreviations: po – pore; ct – cuticle tube; d – dendrites; ds – dendritic sheath; sl – sensillum lymph; lm – lamellae; gl – ganglion. Scale bars: B–G: 1 µm.
Figure 3—figure supplement 4
DPS-T2.
Internal morphology of the pit sensillum 2 (T2) of the dorsal pharyngeal sensilla (DPS). (A) 3D reconstruction of the T2 sensillum. Three sensory neurons (purple) innervate T2. The sensillum shares a terminal pore to the pharyngeal lumen with pit sensilla T1 and T3 (see Figure 3—figure supplements 3 and 5). (B–G) Serial scanning transmission electron microscopy (STEM) sections of the T2 sensillum. (B) The T2 sensillum sits in a small pore at the anterior end of the pharyngeal cavity (ph). (C) Its dendrites extend into the pore through the cuticle channel, together with the T1 and T3 dendrites. (D) Further proximal, a dendritic sheath appears that separates the dendrites of T1 – T3 from each other. (E) The dendrites’ ciliary structures are visible and entirely enclosed by the dendritic sheath(s). The trichogen and tormogen support cells are visible. (F) The dendrites are bathed in the sensillum lymph, but the dendritic sheath is entirely absent at this level. The thecogen and trichogen support cells are visible. (G) Section of the VPS ganglion. The cell bodies of the T2 neurons are visible and lie inside the ganglion. Abbreviations: po – pore; ct – cuticle tube; d – dendrites; ds – dendritic sheath; sl – sensillum lymph; lm – lamellae; gl – ganglion. Scale bars: B–G: 1 µm.
Figure 3—figure supplement 5
DPS-T3.
Internal morphology of the pit sensillum 3 (T3) of the dorsal pharyngeal sensilla (DPS). (A) 3D reconstruction of the T3 sensillum. Four sensory neurons (purple) innervate T3. The sensillum shares a terminal pore to the pharyngeal lumen with pit sensilla T1 and T2 (see Figure 3—figure supplements 3 and 4). (B–G) Serial scanning transmission electron microscopy (STEM) sections of the T3 sensillum. (B) The T3 sensillum sits in a small pore at the anterior end of the pharyngeal cavity (ph). (C) Its dendrites extend into the pore through the cuticle channel, together with the T1 and T2 dendrites. (D) Further proximal, a dendritic sheath appears that separates the dendrites of T1 – T3 from each other. (E) The dendrites’ ciliary structures are visible and entirely enclosed by the dendritic sheath(s). The trichogen and tormogen support cells are visible. (F) The dendrites are bathed in the sensillum lymph, but the dendritic sheath is entirely absent at this level. The thecogen and trichogen support cells are visible. (G) Section of the VPS ganglion. The cell bodies of the T3 neurons are visible and lie inside the ganglion. Abbreviations: po – pore; ct – cuticle tube; d – dendrites; ds – dendritic sheath; sl – sensillum lymph; lm – lamellae; gl – ganglion. Scale bars: B–G: 1 µm.
Figure 3—figure supplement 6
DPS-T4.
Internal morphology of the pit sensillum 4 (T4) of the dorsal pharyngeal sensilla (DPS). (A) 3D reconstruction of the T4 sensillum. Two sensory neurons (purple) innervate T4. The sensillum shares a terminal pore to the pharyngeal lumen with the pit sensillum T5 (see Figure 3—figure supplement 7). (B–G) Serial scanning transmission electron microscopy (STEM) sections of the T4 sensillum. (B) The T4 sensillum sits in a small pore at the posterior end of the pharyngeal cavity (ph). (C) Its dendrites extend into the pore through the cuticle channel, together with the T5 dendrites. (D) Further proximal, a dendritic sheath appears that separates the dendrites of T4 and T5 from each other. The trichogen and tormogen support cells are visible. (E) The dendrites ciliary structures and the thecogen cell are visible; the dendritic sheath is absent at this level. The dendrites are bathed in the sensillum lymph. (F) The sheath cell is highly lamellated at this level. (G) Section of the VPS ganglion. One cell body and one dendrite of the T4 neurons are visible and lie inside the ganglion. Abbreviations: po – pore; ct – cuticle tube; d – dendrites; ds – dendritic sheath; sl – sensillum lymph; lm – lamellae; gl – ganglion. Scale bars: B–G: 1 µm.
Figure 3—figure supplement 7
DPS-T5.
Internal morphology of the pit sensillum 5 (T5) of the dorsal pharyngeal sensilla (DPS). (A) 3D reconstruction of the T5 sensillum. Four sensory neurons (purple) innervate T5. The sensillum shares a terminal pore to the pharyngeal lumen with the pit sensillum T4 (see Figure 3—figure supplement 6). (B–G) Serial scanning transmission electron microscopy (STEM) sections of the T5 sensillum. (B) The T5 sensillum sits in a small pore at the posterior end of the pharyngeal cavity (ph). (C) Its dendrites extend into the pore through the cuticle channel, together with the T4 dendrites. (D) Further proximal, a dendritic sheath appears that separates the dendrites of T4 and T5 from each other. The trichogen and tormogen support cells are visible. (E) The dendrites’ ciliary structures and the thecogen cell are visible; the dendritic sheath is absent at this level. The dendrites are bathed in the sensillum lymph. (F) The sheath cell is highly lamellated at this level. (G) Section of the VPS ganglion. Three cell bodies and one dendrite of the T5 neurons are visible and lie inside the ganglion. Abbreviations: po – pore; ct – cuticle tube; d – dendrites; ds – dendritic sheath; sl – sensillum lymph; lm – lamellae; gl – ganglion. Scale bars: B–G: 1 µm.
Figure 4 with 4 supplements
Main cellular configuration of the dorsal pharyngeal organ (DPO) and posterior pharyngeal sensilla (PPS).
(A) 3D reconstruction of the sensory neurons innervating the DPO. The DPO is a bilaterally organized organ; only the reconstruction of the sensillum on the left is shown. This sensillum is a pit sensillum (T1) that is innervated by two sensory neurons. These are connected through a pore with the pharyngeal lumen. (B) Scanning transmission electron microscopy (STEM) section of the DPO. The sensory neurons innervating the sensilla are highlighted and color-coded for their putative sensory function (purple – gustatory). (C) 3D reconstruction of the sensory neurons innervating the PPS. The PPS is a bilaterally organized organ; only the reconstructions of sensilla on the left are shown. These sensilla are pit sensilla (T1 and T2), innervated by three sensory neurons each. Their pores to the pharyngeal lumen are located in close proximity to each other. (D) STEM section of the PPS. The sensory neurons innervating the sensilla are highlighted and color-coded for their putative sensory function (purple – gustatory). Ultrastructural features of the outer and inner morphology were used to classify the DPO and PPS sensilla. For a detailed description of DPO and PPS sensilla, see Figure 4—figure supplements 1–3. The nomenclature for sensilla was adapted from previous work (Chu-Wang and Axtell, 1972; Rist and Thum, 2017). Abbreviations: d – dorsal; v – ventral; a – anterior; p – posterior; T – pit sensillum. Scale bars: B: 1 µm; D:1 µm.
Figure 4—figure supplement 1
DPO-T1.
Internal morphology of the pit sensillum 1 (T1) of the dorsal pharyngeal organ (DPO). (A) 3D reconstruction of the T1 sensillum. Two sensory neurons (purple) innervate T1. (B–G) Serial scanning transmission electron microscopy (STEM) sections of the T1 sensillum. (B) The terminal pore is visible. (C) The pore is connected to a cuticle channel, which is innervated by the dendrites (D). The two ciliary structures (purple) are visible. A dendritic sheath is present but disintegrating at this level. The tips of the dendrites are bathed in the sensillum lymph, enclosed by the thecogen, trichogen, and tormogen support cells. (E) The two ciliary structures (purple) are visible. The dendritic sheath is absent at this level. (F) The outer dendritic segments pass through the outer support cells. (G) Section of the DPO ganglion (DPOG). The cell bodies of the T1 neurons and of multidendritic neurons A and B are visible. (H+I) Section of the DPOG; the cell body of multidendritic neuron C is visible, from which multiple dendrites extend in the extracellular space toward the muscle cells. Abbreviations: po – pore; ct – cuticle tube; d – dendrites; ds – dendritic sheath; sl – sensillum lymph; lm – lamellae; gl – ganglion. Scale bars: B–H: 1 µm.
Figure 4—figure supplement 2
PPS-T1.
Internal morphology of the pit sensillum 1 (T1) of the posterior pharyngeal organ (PPS). (A) 3D reconstruction of the T1 sensillum. Three sensory neurons (purple) innervate T1. (B–G) Serial scanning transmission electron microscopy (STEM) sections of the T1 sensillum. (B) The terminal pore is visible. (C) The pore is connected to a cuticle channel, which is innervated by the dendrites (D). A dendritic sheath encloses the dendrites but disintegrates at this level. The tips of the dendrites are bathed in the sensillum lymph, enclosed by the thecogen, trichogen, and tormogen support cells. (E) The three ciliary structures (purple) are visible. The dendritic sheath is entirely absent at this level. (F) The outer dendritic segments pass through the thecogen cell, which is highly lamellated. (G) Section of the PPS ganglion (PPSG). The cell bodies of the T1 neurons are visible. Abbreviations: po – pore; ct – cuticle tube; d – dendrites; ds – dendritic sheath; sl – sensillum lymph; lm – lamellae; gl – ganglion. Scale bars: B–G: 1 µm.
Figure 4—figure supplement 3
PPS-T2.
Internal morphology of the pit sensillum 2 (T2) of the posterior pharyngeal organ (PPS). (A) 3D reconstruction of the T2 sensillum. Three sensory neurons (purple) innervate T2. (B–G) Serial scanning transmission electron microscopy (STEM) sections of the T2 sensillum. (B) The terminal pore is visible. (C) The pore is connected to a cuticle channel, which is innervated by the dendrites (D). The dendrites are enclosed by a dendritic sheath (E). The three ciliary structures (purple) are visible. A dendritic sheath is present but disintegrating at this level. The tips of the dendrites are bathed in the sensillum lymph and are enclosed by the thecogen, trichogen, and tormogen support cells. (F) The outer dendritic segments pass through the thecogen cell, which is highly lamellated. (G) Section of the PPS ganglion (PPSG). The cell bodies of the T2 neurons are visible. Abbreviations: po – pore; ct – cuticle tube; d – dendrites; ds – dendritic sheath; sl – sensillum lymph; lm – lamellae; gl – ganglion. Scale bars: B–G: 1 µm.
Figure 4—figure supplement 4
Other internal morphology of the papilla/spot sensilla and chordotonal organs associated with the feeding apparatus.
(A) Schematic drawing of the larval head region highlighting the position of the additional papilla/spot sensilla and chordotonal organs. (B–D) Electron microscopy (EM) images of the dendritic parts of the three papilla/spot sensilla inserting into the pharyngeal lumen. (E, F) EM images of the dendritic parts of the four chordotonal organs associated with the feeding apparatus. Sensilla were identified using prominent structures like a dendritic sheath and a tubular body (papilla/spot sensilla) or a sensory neuron inserted into a scolopale (chordotonal organs). Scale bars: B–H: 1 µm. Abbreviations: D – dorsal; V – ventral; A – anterior; P – posterior; CPS – cephalopharyngeal skeleton; LrN – labral nerve; MxN – maxillary nerve; LbN – labial nerve; ds – dendritic sheath; tb – tubular body; sc – scolopale.
Tables
Table 1
Structural properties of pharyngeal sensilla.
| VPS | DPS | DPO | PPS | ||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| P1 | P2 | Pmod | T1 | H1 | T1 | T2 | T3 | T4 | T5 | P/S1 | P/S2 | T1 | T1 | T2 | |
| Pore | + | + | – | + | – | + | + | + | + | + | – | – | + | + | + |
| Shaft | + | + | + | – | + | – | – | – | – | – | – | – | – | – | – |
| Tube | + | + | – | + | – | + | + | + | + | + | – | – | + | + | + |
| Tubular body | 1 | 1 | 1 | – | 1 | – | – | – | – | – | 1 | 1 | – | – | – |
| Dendrites | 3 | 3 | 1 | 2 | 1 | 2 | 3 | 4 | 2 | 4 | 1 | 1 | 2 | 3 | 3 |
| Lamellae | + | + | – | + | – | (+) | (+) | (+) | + | + | – | – | (+) | + | + |
-
Abbreviations: VPS – ventral pharyngeal sensilla; DPS – dorsal pharyngeal sensilla; DPO – dorsal pharyngeal organ; PPS – posterior pharyngeal sensilla; P – papillum sensillum; Pmod – modified papillum sensillum; T – pit sensillum; H – hair sensillum; P/S – papilla/spot sensillum.
-
+ =structure present; (+) =structure weakly present; – =structure not present.
Table 2
Neuronal composition and putative modality of larval head organs and their nerves.
| Sensilla | Olfactory | Gustatory | Chemo (other) | Thermo | Mechano | Other | Total | Ganglion | Nerve | |
|---|---|---|---|---|---|---|---|---|---|---|
| DO | 7 OS 3 TS 3 P/S | 21 6 5 | – – – | – – – | – 6 – | – – 3 | – – 2 | 21 6 5 | DOG DOG DOG | AN AN AN |
| TOdo | 1 P 1 Pmod 1 P/S | – – – | 3 – – | – – – | – – – | – 1 1 | – – – | 3 1 1 | DOG TOG TOG | AN MxN MxN |
| TOdi | 5T 2 K 3 P 1 P/S | – – – – | 12 – 8 – | – 2 – – | – – – – | 2 – 3 1 | – – – – | 14 2 11 1 | TOG TOG TOG TOG | MxN MxN MxN MxN |
| VO | 1T 3 P/S | – – | 2 – | – – | – – | – 3 | – – | 2 3 | VOG VOG | MxN MxN |
| LO | 2 P/S | – | – | – | – | 2 | – | 2 | LOG | MxN |
| DPS | 5T 2 P/S | – – | 15 – | – – | – – | – 2 | – – | 15 2 | DPSG DPSG | LrN LrN |
| DPO* | 1T | – | 2 | – | – | – | – | 2 | DPOG | LrN |
| PPS | 2T | – | 6 | – | – | – | – | 6 | PPSG | LrN |
| VPS* | 2 P 1 Pmod 1 H 1T | – – – – | 4 – – 2 | – – – – | – – – – | 2 1 1 – | – – – – | 6 1 1 2 | VPSG VPSG VPSG VPSG | LbN LbN LbN LbN |
| P/S – Ext | 1 P/S | – | – | – | – | 1 | – | 1 | – | AN |
| P/S – Ext | 5 P/S | – | – | – | – | 5 | – | 5 | – | MxN |
| P/S – Ph | 3 P/S | – | – | – | – | 3 | – | 3 | – | MxN |
| ChO–DO | 1 | – | – | – | – | 1 | – | 1 | – | AN |
| ChO–TO | 1 | – | – | – | – | 2 | – | 2 | – | MxN |
| ChO–CPS | 1 | – | – | – | – | 1 | – | 1 | – | LrN |
| ChO–Ph | 3 | – | – | – | – | 4 | – | 4 | – | LbN |
| TOTAL | 63 | 21 | 54 | 2 | 6 | 39 | 2 | 124 | ||
| DOG | 14 | 21 | 3 | – | 6 | 3 | 2 | 35 | ||
| TOG | 13 | – | 20 | 2 | – | 8 | – | 30 | ||
| VOG | 4 | – | 2 | – | – | 3 | – | 5 | ||
| LOG | 2 | – | – | – | – | 2 | – | 2 | ||
| DPSG | 7 | – | 15 | – | – | 2 | – | 17 | ||
| DPOG | 1 | – | 2 | – | – | – | – | 2 | ||
| PPSG | 2 | – | 6 | – | – | – | – | 6 | ||
| VPSG | 5 | – | 6 | – | – | 4 | – | 10 | ||
| Single P/S | 9 | – | – | – | – | 9 | 9 | |||
| ChOs | 4 | – | – | – | – | 5 | – | 8 |
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Table updated from Python and Stocker, 2002. This summary presents a synopsis of previously reported cell numbers and identities (Singh and Singh, 1984; Campos-Ortega and Hartenstein, 1985; Schmidt-Ott et al., 1994; Rist and Thum, 2017; Richter et al., 2024), as well as the data presented in this work.
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Abbreviations: DO – dorsal organ; TO – terminal organ; TOdo – dorsal group of the terminal organ; TOdi – distal group of the terminal organ; VO – ventral organ; LO – labial organ; DPS – dorsal pharyngeal sensilla; DPO – dorsal pharyngeal organ; PPS – posterior pharyngeal sensilla; VPS – ventral pharyngeal sensilla; P/S – papilla/spot sensillum; ChO – chordotonal organ; OS – olfactory sensillum; TS – thermosensory sensillum; P – papillum sensillum; Pmod – modified papillum sensillum; T – pit sensillum; K – knob sensillum; H – hair sensillum; DOG – dorsal organ ganglion; TOG – terminal organ ganglion; VOG – ventral organ ganglion; LOG – labial organ ganglion; DPSG – dorsal pharyngeal sensilla ganglion; DPOG – dorsal pharyngeal organ ganglion; PPSG – posterior pharyngeal sensilla ganglion; VPSG – ventral pharyngeal sensilla ganglion; CPS – cephalopharyngeal skeleton; Ph – pharynx; Ext – external; AN – antennal nerve; MxN – maxillary nerve; LrN – labral nerve; LbN – labial nerve.
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*
In the VPS and DPO ganglia, there are three cell bodies of multidendritic neurons each, which in sum is in accordance with previously reported cell numbers. Multidendritic neurons (MDNs) have generally not been considered here; however, based on previously reported cell numbers in the head nerves (Miroschnikow et al., 2018), we propose that there are approximately 25 sensory MDNs (per side) innervating the head region through the MxN, AN, and PaN. Additionally, there are 36 sensory MDNs (in total) projecting through the larval vagus nerve (VN) and innervating the aorta, esophagus, and gut.
Additional files
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Supplementary file 1
Comparison of pharyngeal and cibarial organs in different insect species.
- https://cdn.elifesciences.org/articles/108036/elife-108036-supp1-v1.docx
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MDAR checklist
- https://cdn.elifesciences.org/articles/108036/elife-108036-mdarchecklist1-v1.docx
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Morphology and ultrastructure of pharyngeal sense organs of Drosophila larvae
eLife 14:RP108036.
https://doi.org/10.7554/eLife.108036.3
