Desmosomal connectomics of all somatic muscles in an annelid larva
- Living Systems Institute, University of Exeter, United Kingdom
- Janelia Research Campus, United States
- kazmos GmbH, Germany
Figures
Figure 1 with 3 supplements
Whole-body desmosomal connectomics in the Platynereis larva.
(A) Stylised scanning electron micrograph of a 3-day-old Platynereis larva with the main body regions indicated. (B) Skeleton representation of the aciculae and all muscle cells in the larva, …
Figure 1—figure supplement 1
Desmosome and muscle ultrastructure.
(A) Desmosomes between aciculoblast and muscle cells. (B) Hemidesmosomes formed on the midline extracellular matrix by the axochord, the oblique muscles, and the midline cells. Tonofibrils connected …
Figure 1—figure supplement 2
Cells containing desmosomes, tonofibrils, or both.
(A) Percentage of cells containing desmosomes, tonofibrils or, both, or neither, arranged by cell type. Bars represent the fraction of cells with desmosomes, tonofibrils, both or neither. The …
Figure 1—figure supplement 3
Morphological renderings of non-muscle components of the desmosomal connectome.
Aciculae and acicular follicle cells. (B) Chaetae and the four types of chaetal follicular cells. The region in the inset is shown in C. (C) Close-up of the left parapodium in the second segment …
Figure 2
Classification and distribution of muscle cell types in the 3-day-old Platynereis larva.
(A) Morphological rendering of traced skeletons and soma position (spheres) of all acicular muscles. The table shows the cell-type classification of acicular muscles. (B) All anterior oblique …
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Figure 2—source data 1
Source data for panel I listing the segmental and left–right distribution of all muscle cell types.
- https://cdn.elifesciences.org/articles/71231/elife-71231-fig2-data1-v2.csv
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Figure 2—source data 2
All muscle skeletons as point clouds with tangent vectors (dotprop).
An R data source file (.RDS).
- https://cdn.elifesciences.org/articles/71231/elife-71231-fig2-data2-v2.zip
Figure 3 with 1 supplement
The desmosome connectome of the 3-day-old Platynereis larva.
(A) The desmosomal connectome coloured by Leiden modules. Nodes represent cells or basal lamina fragments and edges represent desmosomal connections. Node sizes are proportional to weighted degree …
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Figure 3—source data 1
The desmosomal connectome graph in igraph format.
- https://cdn.elifesciences.org/articles/71231/elife-71231-fig3-data1-v2.zip
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Figure 3—source data 2
The desmosomal connectome graph in visNetwork format.
- https://cdn.elifesciences.org/articles/71231/elife-71231-fig3-data2-v2.txt
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Figure 3—source data 3
The desmosomal connectome graph in html format.
- https://cdn.elifesciences.org/articles/71231/elife-71231-fig3-data3-v2.zip
Figure 3—figure supplement 1
Grouped connectivity graph of the desmosomal connectome.
Nodes represent groups of cells grouped by cell type. Basal body and other fragments are not shown for clarity. Node size is proportional to degree, edge thickness to the square root of edge weight …
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Figure 3—figure supplement 1—source data 1
The grouped desmosomal connectome graph in visNetwork format.
- https://cdn.elifesciences.org/articles/71231/elife-71231-fig3-figsupp1-data1-v2.txt
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Figure 3—figure supplement 1—source data 2
The grouped desmosomal connectome graph in html format.
- https://cdn.elifesciences.org/articles/71231/elife-71231-fig3-figsupp1-data2-v2.zip
Figure 4
Network statistics of the desmosomal connectome relative to random graphs.
(A) Degree distribution and (B) edge-weight distribution of the desmosomal connectome compared to the synaptic (neuronal) connectome (neuro), scale-free (sf), Erdős-Rényi (erdos), and …
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Figure 4—source data 1
Network statistics for the 1,000 simulated scale-free, Erdős-Rényi, preferential-attachment graphs and the 1000 subsampled desmosomal connectome and synaptic connectome graphs.
- https://cdn.elifesciences.org/articles/71231/elife-71231-fig4-data1-v2.txt
Figure 5
Local connectivity of the desmosomal connectome.
(A) Morphological rendering of cells of the desmosomal connectome in the midline (black) and on the right (cyan) and left (orange) side of the body. (B) The same cells in the force-field-based …
Figure 6 with 4 supplements
Cell-type diversity and connectivity of the parapodial muscle complex.
(A) Morphological rendering of all cells of the desmosomal connectome with a weighted degree >10. (B) Same cells coloured with a colour scale proportional to the cell’s weighted degree, ventral and …
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Figure 6—source data 1
Source data for panel E of Figure 6.
Text file listing weighted degree values for the most highly connected cells in the desmosomal connectome, arranged by cell class.
- https://cdn.elifesciences.org/articles/71231/elife-71231-fig6-data1-v2.txt
Figure 6—figure supplement 1
Ultrastructure of chaetal sac cells.
(A) Soma positions of chaetoblast and follicle cells. Each chaeta, growing from a chaetoblast cell is accompanied by two chaeFC-hemi, one chaeFC-ER, one chaeFC-noER, and one chaeFC-EC cell. (B) TEM …
Figure 6—figure supplement 2
Morphological renderings of oblique muscles.
(A) Lateral and (B) posterior views of a parapodium (second segment, left side) with a neuropodial and notopodial lobe and a spinning gland. (C) All anterior oblique muscles. Outline of (D) …
Figure 6—figure supplement 3
Morphological renderings of acicular and chaetal muscles.
(A) Posterior view of a parapodium (second segment, left side) with all acicular muscles shown. (B) Outline of MUSac-neuAV, (C) MUSac-neuPV, (D) MUSac-neuDy, (E) MUSac-neuPD, (F) MUSac-neuDach, (G) …
Figure 6—figure supplement 4
Morphological renderings of muscles in the parapodial muscle complex and inferred movement of the aciculae.
(A) Skeleton view of the parapodial muscle complexes in all three parapodia. Each parapodium has a notopodial (dorsal) and a neuropodial (ventral) acicula. (B) The MUSobP-neu muscles (neuDdist, …
Figure 7 with 1 supplement
Acicula tracking, muscle contractions, and desmosomal connectivity.
(A) Acicular position over time in all six parapodia analysed from video tracking data to indicate gait of the larva over time. Angles between the anterior–posterior bodyline connecting the mouth …
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Figure 7—source data 1
Source data for panel A-G of Figure 7.
- https://cdn.elifesciences.org/articles/71231/elife-71231-fig7-data1-v2.gz
Figure 7—figure supplement 1
Somatic muscles in Platynereis larvae visualised by phalloidin Images are maximum intensity projections of CLSM-image stacks taken of phalloidin-labelled specimens.
(A) Three-day-old larva in whole-body dorsal overview, detail of contracted neuro- (B) and notopodia (C) in dorsal view; (D) 4-day-old larva in whole-body dorsal overview (with dorsolateral …
Figure 8 with 1 supplement
Combining synaptic and desmosomal connectomics.
(A) Graph representation of motoneuron synaptic inputs to the desmosomal connectome. The 11 main motoneuron groups are shown. (B) Sankey diagram of the synaptic innervation of muscle types by …
Figure 8—figure supplement 1
Downstream synaptic and desmosomal partners of main motoneuron types.
(A–J) Morphological renderings of muscle targets of 10 trunk motoneuron types (blue) in the 3-day-old larva, their postsynaptic muscle targets (orange-red) and the desmosomal partners of the …
Figure 9
Combined synaptic–desmosomal graphs of motoneurons.
Synaptic connections (orange arrows) of motoneuron classes to muscles and desmosomal links (blue edges) of the innervated muscle cells. Combined synaptic-desmosomal graph for (A) MNantelope, (B) …
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Figure 9—source data 1
A zip archive of CATMAID json files.
The graphs can be loaded in the CATMAID graph widget at https://catmaid.jekelylab.ex.ac.uk.
- https://cdn.elifesciences.org/articles/71231/elife-71231-fig9-data1-v2.zip
Figure 10
Postsynaptic muscle targets in the parapodial complex of different motoneurons.
Morphological rendering of postsynaptic muscle targets (red-purple) within the parapodial complex of (A) MNcrab, (B) MNbiramous, (C) MNwave, (D) MNspider-ant, (E) MNspider-post, (F) MNhose, (G) …
Videos
Video 1
All muscles in the 3-day-old Platynereis larva.
Individual muscle cell types are shown by cell type and muscle category. The 12 aciculae are shown in grey for reference. The cell nuclei are labelled by a sphere. The yolk and body outlines are …
Video 2
Muscle groups in the parapodial complex.
Reconstruction of all cell groups in the left parapodial complex in the second segment. The neuropodial and notopodial aciculae are shown in black, chaetae are in yellow. The dark-brown cell with …
Video 3
3D visualisation of all cells in the desmosomal connectome coloured by module.
The colour scheme is the same as in Figure 3. The cell nuclei are labelled by a sphere. Individual Z planes from the stack are also shown to indicate the orientation of the serial EM stack. The yolk …
Video 4
3D visualisation of selected muscle groups and their desmosomal connections.
Morphological renderings of selected muscle groups and partner cells and the desmosomes (in red) that connect them. The video illustrates that desmosomes often occur at the most distal ends of …
Video 5
Acicular movements in crawling and startling Platynereis larvae.
Differential interference contrast (DIC) video of a crawling larva and a startling larva (end of the video) with the position of the aciculae tracked by DeepLabCut.
Video 6
Calcium imaging of muscle contractions in Platynereis larvae.
Spontaneous contractions of individual muscle groups as visualised by the confocal imaging of calcium signals reported by GCaMP6s fluorescence. The larvae were also imaged in the differential …
Video 7
3D visualisation of motoneurons, their muscle targets, and the desmosomal partners of the muscles.
The first half of the video shows the combined synaptic and desmosomal connectome of different types of motoneurons. The muscles postsynaptic to the motoneurons are shown in orange. The desmosomal …
Tables
Table 1
Muscle cell types.
Hierarchical classification and nomenclature of all muscle cells in the 3-day-old Platynereis larva.
| Anatomical name and CATMAID annotation | Example CATMAID neuron name (example) | Number of cells (per segment [sg] and body side) | Desmosomal connections to | Synaptic connections from (>3 synapses) | ||
|---|---|---|---|---|---|---|
| Acicular muscle (MUSac) | Notopodial | Anterior notopodial acicular muscle | MUSac-notA | sg1: 2 l, 2 r sg2: 2 l, 2 r sg3: 2 l, 2 r | Proximal base of notopodial acicula; notopodial ECs | MNring, MNcrab, MNwave, MNantacic |
| Posterior notopodial acicular muscle | MUSac-notP | sg1: 2 l, 2 r sg2: 2 l, 2 r sg3: 2 l, 2 r | Proximal base of notopodial acicula; septal ECs and dorsal paratroch | MNacic, MNwave, MNbow, MNspider-ant, MNcrab, MNperif | ||
| Middle notopodial acicular muscle | MUSac-notM | sg1: 2 l, 2 r sg2: 2 l, 2 r sg3: 2 l, 2 r | Proximal base of notopodial acicula; parapodial ECs | MNwave, MNacic, MNantaci, MNbow | ||
| Unpaired notopodial dorsal acicular muscle | MUSac-notDo | sg1: 0 l, 0 r sg2: 1 l, 0 r sg3: 0 l, 0 r | Proximal base of notopodial acicula; dorsal ECs | None | ||
| Neuropodial | Anterior ventral neuropodial acicular muscle | MUSac-neuAV | sg1: 2 l, 2 r sg2: 3 l, 3 r sg3: 3 l, 3 r | Proximal base of neuropodial acicula; epidermal cells near ventrolateral muscles | MNcrab, MNring, MNchae | |
| Posterior dorsal neuropodial acicular muscle | MUSac-neuPD | sg1: 3 l, 3 r sg2: 3 l, 3 r sg3: 3 l, 3 r | Proximal base of neuropodial acicula; dorsal ECs and notopodial EC chaeFC and distal notopodial acicula (1) and dorsal paratroch (2) | MNarm, sparse various others | ||
| Posterior ventral neuropodial acicular muscle | MUSac-neuPV | sg1: 2 l, 2 r sg2: 3 l, 3 r sg3: 2 l, 2 r | Proximal base of neuropodial acicula; ventral paratroch and ECs around it | MNcrab, MNacicX, MNperifac, MNspider-post, MNspider-ant, MNpostv | ||
| Neuropodial Y | MUSac-neuDy | sg1: 0 l, 0 r sg2: 1 l, 1 r sg3: 1 l, 1 r | Proximal and mid neuropodial acFC; neuropodial chaeFC-hemi; mid-parapodial septal EC | Fragments | ||
| Dorsal neuropodial muscle to notopodium | MUSac-neuDx | sg1: 0 l, 0 r sg2: 2 l, 2 r sg3: 2 l, 2 r | Proximal neuropodial acFC; mid-distal notopodial acFC; and mid-dorsal parapodial ECs (2) | MNchae, MNcrab, MNarm | ||
| Dorsal neuropodial chaetal muscle | MUSac-neuDach | sg1: 3 l, 3 r sg2: 3 l, 3 r sg3: 3 l, 3 r | Entire length of neuropodial acicula (all acFC); mid-parapodial ECs | MNarm, MNac, MNchae, MNantacic | ||
| Chaetal sac retractor | MUSac-neure | sg1: 1 l, 1 r sg2: 2 l, 2 r sg3: 1 l, 1 r | Proximal base of neuropodial acicula; proximal neuropodial chaeFC | Sparse | ||
| Inter-acicular | interacicular_muscle | MUSac-i | sg1: 1 l, 1 r sg2: 1 l, 1 r sg3: 1 l, 1 r | Proximal base of neuropodial acicula; proximal base of notopodial acicula | None | |
| Anterior oblique muscle | Anterior ventral oblique muscles | Parapodial retractor muscle | MUSobA-re | sg1: 6 l, 5 r sg2: 7 l, 7 r sg3: 7 l, 7 r | Neuropodial EC chaeFC and chaetal sac ECs; midline cells | MNspider-ant, MNantacic, MNhose, MNob-contra |
| Ventral parapodial muscle arc | MUSobA-arc | sg1: 2 l, 2 r sg2: 4 l, 4 r sg3: 3 l, 3 r | Basal lamina next to nerve chord; neuropodial ECs and chaeFC-ECs | MNspider-ant, MNantacic, MNob-contra | ||
| Medial oblique to mid-parapodium | MUSobA-mpp | sg1: 1 l, 1 r sg2: 2 l, 2 r sg3: 3 l, 3 r | Medial basal lamina next to medial nerve cord and putative radial glia; mid-parapodial ECs | MNob-contra, MNhose, MNcrab, others | ||
| Mediolateral oblique to mid-parapodium | MUSobA-mlpp | sg1: 0 l, 0 r sg2: 2 l, 2 r sg3: 0 l, 0 r | Medial basal lamina next to mediolateral nerve cord and putative radial glia; mid-parapodial ECs | MNhose | ||
| Lateral oblique to mid-parapodium | MUSobA-lpp | sg1: 1 l, 1 r sg2: 2 l, 2 r sg3: 2 l, 2 r | Lateral basal lamina next to the nerve cord and putative radial glia; mid-parapodial ECs | MNob-contra, MNhose, MNsmile, other | ||
| Oblique to start of transverse | MUSobA-trans | sg1: 1 l, 1 r sg2: 2 l, 2 r sg3: 2 l, 2 r | Basal lamina next to the axochord; ventrolateral ECs | MNhose, MNcross | ||
| Posterior oblique muscle | Posterior dorsal oblique muscle | Notopodial dorsal oblique muscle | MUSobP-notD | sg1: 4 l, 4 r sg2: 5 l, 5 r sg3: 5 l, 5 r | Dorsal longitudinal muscles and ECs near them; ECs of the notopodium | MNpostacic, MNspider-ant |
| Neuropodial dorsal oblique long | MUSobP-neuDlong | sg1: 1 l, 1 r sg2: 2 l, 2 r sg3: 2 l, 1 r | MUSlong_D; distal neuropodial acFC, neuropodial ECs, and mid-parapodial ECs | MNspider-post; MNpostacic | ||
| Neuropodial dorsal oblique proximal | MUSobP-neuDprox | sg1: 3 l, 3 r sg2: 3 l, 3 r sg3: 3 l, 3 r | MUSlong_D; dorsal paratroch and ECs around it | MNspider-post | ||
| Neuropodial dorsal oblique distal | MUSobP-neuDdist | sg1: 3 l, 3 r sg2: 3 l, 3 r sg3: 3 l, 3 r | ECs near dorsal paratroch; distal neuropodial acFC, neuropodial ECs and mid-parapodial ECs | MNbow | ||
| Posterior ventral oblique muscle | Posterior ventral neuropodial muscle | MUSobP-neuV | sg1: 5 l, 5 r sg2: 7 l, 7 r sg3: 7 l, 7 r | Basal lamina next to VNC; ECs from the distal part of neuropodial acicula to the ventral paratroch area | MNring, MNspider-post, MNob-ipsi, MN_oblique, MNob, many fragments | |
| Posterior ventral notopodial muscle | MUSobP-notV | sg1: 3 l, 3 r sg2: 3 l, 3 r sg3: 3 l, 3 r | Basal lamina next to VNC; septal ECs; EC and chaeFC near distal part of notopodial acicula | MNhose, MNspider-post, MNob-ipsi, MN_oblique, MNladder, MNob-contra, fragments | ||
| Oblique to distal inter-acicular | MUSobP-M | sg1: 0 l, 0 r; sg2: 1 l, 1 r sg3: 1 l, 1 r | Each other and basal lamina of the VNC; distal inter-acicular muscle | None | ||
| Oblique to body wall near distal inter-acicular and neuropodial Y | MUSobP-noty | sg1: 1 l, 1 r sg2: 1 l, 1 r sg3: 1 l, 1 r | Basal lamina next to the axochord; septal ECs | MNhose, MNpostacic, MNob-ipsi, MNspider-post, fragments | ||
| sg0 ventral posterior oblique muscle | MUSobP | sg0: 2 l, 2 r sg1: 0 l, 0 r sg2: 0 l, 0 r sg3: 0 l, 0 r | Basal lamina near VNC and ventral ECs; dorsal ECs | MNsmile, MNcrab, MNob-contra, MNmouth | ||
| Posterior median oblique muscle | Distal inter-acicular muscle | MUSobP-i | sg1: 1 l, 1 r sg2: 1 l, 1 r sg3: 1 l, 1 r | Neuropodial EC, chaeFC-EC, acFC-EC; notopodial EC, chaeFC EC; MUSob-postM | Sparse | |
| Oblique muscle other | MUSob | sg0: 1 l, 1 r sg1: 0 l, 0 r sg2: 0 l, 0 r sg3: 0 l, 0 r | ECs near mouth/lower lip; MUStrans | MNsmile | ||
| Chaetal sac muscle | Notopodial | Notochaetal next to dorsal oblique | MUSchae-notDob | sg1: 3 l, 3 r sg2: 3 l, 3 r sg3: 3 l, 3 r | Dorsolateral ECs; notopodial chaeFC | MNpostatic, various |
| Dorsal notopodial chaetal sac muscle | MUSchae-notD | sg1: 1 l, 1 r sg2: 1 l, 1 r sg3: 1 l, 1 r | Proximal notopodial acicula; notopodial chaeFC (semicircle around dorsal side of notopodial chaetal sac) | Sparse | ||
| Next to dorsal notopodial chaetal sac muscle | MUSchae-notDn | sg1: 1 l, 1 r sg2: 1 l, 1 r sg3: 1 l, 1 r | Dorsolateral ECs; ECs of the notopodial chaetal sac and notopodial chaeFC-ECs; notopodial acFC cells | MNpostacic | ||
| Anterior notopodial chaetal sac muscle | MUSchae-notA | sg1: 1 l, 1 r sg2: 1 l, 1 r sg3: 1 l, 1 r | Mid-parapodial chaetal sac ECs and MUSobA-che; notopodial ECs, chaeFC-EC and acFC | MNspider-ant, MNantacic | ||
| Notopodial chaetal muscle under acicula | MUSchae-notAac | sg1: 4 l, 4 r sg2: 4 l, 4 r sg3: 4 l, 4 r | Distal acFC; all types of chaetal sac cells | MNcrab, MNbiramous, MNwave, MNantacic, MNacic, MNspider-ant, MNbow, fragments | ||
| Notopodial retractor muscle | MUSchae-notAre | sg1: 0 l, 0 r sg2: 1 l, 1 r sg3: 1 l, 1 r | Mid-parapodial ECs; distal notopodial acFC and EC chaeFC | Sparse | ||
| Neuropodial | Neurochaetal next to ventral oblique | MUSchae-neuVob | sg1: 2 l, 2 r sg2: 3 l, 3 r sg3: 2 l, 2 r | Proximal neuropodial chaeFC-hemi; ventrolateral ECs | MNchae | |
| Neuropodial chaetal muscle under acicula | MUSchae-neuDac | sg1: 4 l, 4 r sg2: 5 l, 5 r sg3: 5 l, 5 r | Mid and distal neuropodial circumacicluar cells; proximal and distal chaeFC cells and chaetal sac ECs | MNbiramous, MNchae, MNspider-ant, fragments | ||
| Anterior ventral neurochaetal muscle ob | MUSchae-neuAVo | sg1: 2 l, 2 r sg2: 3 l, 3 r sg3: 3 l, 3 r | Neuropodial mid acFC and proximal chaeFC; distal chaeFC and neuropodial ECs | MNarm, MNchae | ||
| Anterior ventral neurochaetal muscle trans | MUSchae-neuAVt | sg1: 1 l, 1 r sg2: 1 l, 1 r sg3: 1 l, 1 r | Distal neuropodial acFC; ventrolateral ECs next to VLM | MNacicX, MNspider-post | ||
| Chaetal sac under parapodial retractor | MUSchae-Are | sg1: 1 l, 1 r sg2: 1 l, 1 r sg3: 1 l, 1 r | Mid and distal neuropodial chaeFC cells | MNbiramous, MNspider-ant | ||
| Transverse muscle | Transverse muscle | MUStrans | sg0: 4 l, 5 r sg1: 5 l, 5 r sg2: 9 l, 9 r sg3: 8 l, 9 r pyg: 4 l, 4 r | Lateral ECs; metatroch; akrotroch | MNring, MNhose, MNsmile, MNob-contra, MNladder | |
| Longitudinal muscle | Dorsolateral | Dorsolateral muscle | MUSlongD | sg0: 11 l, 15 r sg1: 13 l, 15 r sg2: 10 l, 10 r sg3: 7 l, 7 r | Epidermal cells; MUSobP-neuD, MUSobP-notDprox, MUSobP-notDlong; paratroch; nuchal organ | MN2, MNring, MNcrab |
| Ventrolateral | Ventrolateral muscle | MUSlongV | head: 9 l, 8 r, 1 m sg0: 7 l, 4 r sg1: 8 l, 12 r sg2: 11 l, 8 r sg3: 7 l, 7 r pyg: 1 l, 1 r | Basal lamina lateral of VNC; ventral ECs | MN1, MNring, MNcrab, MNsmile, MNspider-ant | |
| Axochord | Axochord | MUSax | sg1: 4 l, 4 r sg2: 1 l, 1 r sg3: 1 l, 1 r | Basal lamina next to VNC; radial glia-like midline; ECs | MNax; MNsmile | |
| Digestive system muscle | Circular pygidial muscle | MUSring-pyg | pyg1 | Self; dorsal pygidial ECs; ventral pygidial ECs | None | |
| Pharyngeal muscle | MUSph | 28 l, 30 r | Basal lamina | None | ||
| Lower lip muscle | MUSll | 5 l, 5 r | Metatroch and ECs next to metatroch | MNsmile | ||
| Head muscle | Head appendage | Antenna muscle | MUSant | 4 l, 4 r | ECs | Sparse |
| Lyrate muscle | MUSly | 3 l, 3 r | Basal lamina | None | ||
| Palp muscle | MUSpl | 2 l, 2 r | ECs and prototroch cover cells | None | ||
| Cirrus muscle | MUSci | 2 l, 2 r | ECs and basal lamina | None | ||
| Other head | Cheek muscle | MUSch | 3 l, 3 r | Basal lamina | MNsmile | |
| Plexus muscle | MUSpx | 1 | ECs and putative glia | SNs with very weak connections | ||
| Ventral transverse muscle of prostomium | MUSpr-Vt | 1 | Dorsolateral head ECs | Sparse | ||
| Triangle muscle | MUStri | 1 l, 1 r | Basal lamina | None | ||
| Smooth head muscles | MUSmed-head | 1 l, 1 r | Head ECs | None |
