Three consecutive generations of nephridia occur during development of <i>Platynereis dumerilii</i> (Annelida, Polychaeta)

Hasse, Christian; Rebscher, Nicole; Reiher, Wencke; Sobjinski, Kathrin; Moerschel, Erhard; Beck, Lothar A.; Tessmar-Raible, Kristin; Arendt, Detlev; Hassel, Monika

doi:10.1002/dvdy.22331

Cited by 10 publications

(11 citation statements)

References 29 publications

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“…The larval nephridium (also called ciliated protonephridia (Hasse et al, 2010)) is found adjacent to the longitudinal muscles, located laterally between the 2nd and 3rd larval segments (Figure 1E, Figure 2D, Supplementary Figure 1B). It is composed of 7 cells on each side of the body which connect to the coelomic cavity.…”

Section: Resultsmentioning

confidence: 99%

“…To evaluate the quality of cellular segmentation, we focused on the larval nephridia ( Figure 2D). Previous transmission EM analysis had shown that the larval nephridia are embedded between the body surface muscles and oblique muscles, and that the tubule wall is formed from single cells wrapping around a tight lumen with six cilia constantly present (Hasse et al, 2010). However, transmission EM on single sections could not resolve how many cells contribute to this structure and how many distinct cilia they protrude into the lumen.…”

Section: Segmentation Of Nuclei Cells Tissues and Body Partsmentioning

confidence: 97%

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Whole-body integration of gene expression and single-cell morphology

Vergara

Pape

Meechan

et al. 2020

Preprint

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Animal bodies are composed of hundreds of cell types that differ in location, morphology, cytoarchitecture, and physiology. This is reflected by cell type-specific transcription factors and downstream effector genes implementing functional specialisation. Here, we establish and explore the link between cell type-specific gene expression and subcellular morphology for the entire body of the marine annelid Platynereis dumerilii. For this, we registered a whole-body cellular expression atlas to a high-resolution electron microscopy dataset, automatically segmented all cell somata and nuclei, and clustered the cells according to gene expression or morphological parameters. We show that collective gene expression most efficiently identifies spatially coherent groups of cells that match anatomical boundaries, which indicates that combinations of regionally expressed transcription factors specify tissue identity. We provide an integrated browser as a Fiji plugin to readily explore, analyse and visualise multimodal datasets with remote ondemand access to all available datasets. Figure 1: Ultrastructure of a whole Platynereis by serial block-face scanning electron microscopy.A: The 3D SBEM dataset can be observed in multiple orientations, either along the acquisition plane (transversal plane, top row) or as orthogonal projections (horizontal plane, bottom row; scale bar: 50 µm). B-E: fine ultrastructure is revealed when exploring the datasets at native resolution (10 nm pixel-size x/y; scale bars: 2 µm). B: epithelial cell, interfacing the cuticle and the underlying muscle. Bundles of cytoskeletal filaments (arrowhead) form part of the attachment complex (inset). C: the adult eye forms a pigment cup composed of pigment cells (PiC) and rhabdomeric photoreceptors (rPRC). The photoreceptors extend a distal segment made by microvillar projections (mi) for light detection. In the centre of the pigment cup is the vitreous body (vb). D: longitudinal muscle fibres are cut transversally displaying cross-sections of the sarcomere as well as of the sarcoplasmic reticulum that contacts the plasma membrane (inset). E: cross section of the distal part of the nephridia, highlighting the autocell junction (arrow) which forms a lumen. The lumen houses a bundle of motile cilia (identified by the 9+2 microtubule arrangement, inset), which are contributed by each cell of the nephridium, noted by the presence of basal bodies. Panels B to E are snapshots selected from the full volume and can be retrieved directly from the PlatyBrowser "Bookmark" function. Supplementary Figure 2A). Figure 2 gives a few examples of the achieved segmentation quality for epidermal cells (B), muscles (C) and nephridia (D). We measured nuclei sizes to range from 33.6 to 147.5 cubic microns, and cell sizes from 59.8 to 1224.6 cubic microns. Note that neurites in the neuropil have not been segmented, as they are not sufficiently preserved in the EM volume for automated segmentation. Figure 2: Segmentation of nuclei, cells, tissues and body parts.A. Cells and nuclei ar...

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Section: Resultsmentioning

confidence: 99%

Section: Segmentation Of Nuclei Cells Tissues and Body Partsmentioning

confidence: 97%

Whole-body integration of gene expression and single-cell morphology

Vergara

Pape

Meechan

et al. 2020

Preprint

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“…Invertebrate alkaline phosphatases appear to have a similar association with transport: ALP activity has been reported in excretory organs of insects and annelids, salivary glands of insect larvae, and the guts of diverse species (Myohara, 2004;Eguchi, 1995;Hasse et al, 2010;Kitamura and Shimizu, 2000).…”

Section: Introductionmentioning

confidence: 85%

“…In other annelids, alkaline phosphatases display fairly restricted activity both in space and in developmental time. Although Kitamura and Shimizu (2000) and Hasse et al, (2010) are studies of embryos and juveniles, Myohara's (2004) observations on adult E. japonensis worms suggest that widespread ALP activity in mesodermal tissues is, at the very least, not a universal feature of annelids. Interestingly, alkaline phosphatase activity in muscle tissue of a euryhaline crustacean appears to respond to changes in environmental salinity (Pinoni et al, 2005).…”

Section: Discussionmentioning

confidence: 99%

The dynamics of alkaline phosphatase activity during operculum regeneration in the polychaete Pomatoceros lamarckii

Szabó¹,

Ferrier²

2014

Int. J. Dev. Biol.

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Alkaline phosphatase enzymes are found throughout the living world and fulfil a variety of functions. They have been linked to regeneration, stem cells and biomineralisation in a range of animals. Here we describe the pattern of alkaline phosphatase activity in a spiralian appendage, the operculum of the serpulid polychaete Pomatoceros lamarckii. The P. lamarckii operculum is reinforced by a calcified opercular plate and is capable of rapid regeneration, making it an ideal model system to study these key processes in annelids. Alkaline phosphatase activity is present in mesodermal tissues of both intact and regenerating opercular filaments, in a strongly regionalised pattern correlated with major morphological features. Based on the lack of epidermal activity and the broad distribution of staining in mesodermal tissues, calcification-or stem cell-specific roles are unlikely. Transcriptomic data reveal that at least four distinct genes contribute to the detected activity. Opercular alkaline phosphatase activity is sensitive to levamisole. Phylogenetic analysis of metazoan alkaline phosphatases indicates homology of the P. lamarckii sequences to other annelid alkaline phosphatases, and shows that metazoan alkaline phosphatase evolution was characterised by extensive lineage-specific duplications.

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“…In addition, both types do occur subsequently during ontogeny in certain polychaetes (e.g. [42]). The finding of a cilium in a podocyte of Lepidochitona corrugata – remarkably the first report of a podocyte bearing a cilium in a mollusc – lends substantial support to this concept.…”

Section: Discussionmentioning

confidence: 99%

Development of the excretory system in a polyplacophoran mollusc: stages in metanephridial system development

2012

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BackgroundTwo types of excretory systems, protonephridia and metanephridial systems are common among bilaterians. The homology of protonephridia of lophotrochozoan taxa has been widely accepted. In contrast, the homology of metanephridial systems – including coelomic cavities as functional units – among taxa as well as the homology between the two excretory systems is a matter of ongoing discussion. This particularly concerns the molluscan kidneys, which are mostly regarded as being derived convergently to the metanephridia of e.g. annelids because of different ontogenetic origin. A reinvestigation of nephrogenesis in polyplacophorans, which carry many primitive traits within molluscs, could shed light on these questions.ResultsThe metanephridial system of Lepidochitona corrugata develops rapidly in the early juvenile phase. It is formed from a coelomic anlage that soon achieves endothelial organization. The pericardium and heart are formed from the central portion of the anlage. The nephridial components are formed by outgrowth from lateral differentiations of the anlage. Simultaneously with formation of the heart, podocytes appear in the atrial wall of the pericardium. In addition, renopericardial ducts, kidneys and efferent nephroducts, all showing downstream ciliation towards the internal lumen, become differentiated (specimen length: 0.62 mm). Further development consists of elongation of the kidney and reinforcement of filtration and reabsorptive structures.ConclusionsDuring development and in fully formed condition the metanephridial system of Lepidochitona corrugata shares many detailed traits (cellular and overall organization) with the protonephridia of the same species. Accordingly, we suggest a serial homology of various cell types and between the two excretory systems and the organs as a whole. The formation of the metanephridial system varies significantly within Mollusca, thus the mode of formation cannot be used as a homology criterion. Because of similarities in overall organization, we conclude that the molluscan metanephridial system is homologous with that of the annelids not only at the cellular but also at the organ level.

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Three consecutive generations of nephridia occur during development of Platynereis dumerilii (Annelida, Polychaeta)

Cited by 10 publications

References 29 publications

Whole-body integration of gene expression and single-cell morphology

Whole-body integration of gene expression and single-cell morphology

The dynamics of alkaline phosphatase activity during operculum regeneration in the polychaete Pomatoceros lamarckii

Development of the excretory system in a polyplacophoran mollusc: stages in metanephridial system development

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