ALBERT

Description: Cell lineage, cell cycle, and cell fate are tightly associated in developmental processes, but in vivo studies at single-cell resolution showing the intricacies of these associations are rare due to technical limitations. In this study on the marine annelid Platynereis dumerilii, we investigated the lineage of the 4d micromere, using high-resolution long-term live imaging complemented with a live-cell cycle reporter. 4d is the origin of mesodermal lineages and the germline in many spiralians. We traced lineages at single-cell resolution within 4d and demonstrate that embryonic segmental mesoderm forms via teloblastic divisions, as in clitellate annelids. We also identified the precise cellular origins of the larval mesodermal posterior growth zone. We found that differentially-fated progeny of 4d (germline, segmental mesoderm, growth zone) display significantly different cell cycling. This work has evolutionary implications, sets up the foundation for functional studies in annelid stem cells, and presents newly established techniques for live imaging marine embryos.

Description: Background During early development, patterns of cell division—embryonic cleavage—accompany the gradual restriction of blastomeres to specific cell fates. In Spiralia, which include annelids, mollusks, and flatworms, “spiral cleavage” produces a highly stereotypic, spiral-like arrangement of blastomeres and swimming trochophore-type larvae with rotational (spiral) symmetry. However, starting at larval stages, spiralian larvae acquire elements of bilateral symmetry, before they metamorphose into fully bilateral juveniles. How this spiral-to-bilateral transition occurs is not known and is especially puzzling for the early differentiating brain and head sensory organs, which emerge directly from the spiral cleavage pattern. Here we present the developmental cell lineage of the Platynereis larval episphere. Results Live-imaging recordings from the zygote to the mid-trochophore stage (~ 30 hpf) of the larval episphere of the marine annelid Platynereis dumerilii reveal highly stereotypical development and an invariant cell lineage of early differentiating cell types. The larval brain and head sensory organs develop from 11 pairs of bilateral founders, each giving rise to identical clones on the right and left body sides. Relating the origin of each bilateral founder pair back to the spiral cleavage pattern, we uncover highly divergent origins: while some founder pairs originate from corresponding cells in the spiralian lineage on each body side, others originate from non-corresponding cells, and yet others derive from a single cell within one quadrant. Integrating lineage and gene expression data for several embryonic and larval stages, we find that the conserved head patterning genes otx and six3 are expressed in bilateral founders representing divergent lineage histories and giving rise to early differentiating cholinergic neurons and head sensory organs, respectively. Conclusions We present the complete developmental cell lineage of the Platynereis larval episphere, and thus the first comprehensive account of the spiral-to-bilateral transition in a developing spiralian. The bilateral symmetry of the head emerges from pairs of bilateral founders, similar to the trunk; however, the head founders are more numerous and show striking left-right asymmetries in lineage behavior that we relate to differential gene expression.

Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Özpolat, B. D., Randel, N., Williams, E. A., Bezares-Calderón, L. A., Andreatta, G., Balavoine, G., Bertucci, P. Y., Ferrier, D. E. K., Gambi, M. C., Gazave, E., Handberg-Thorsager, M., Hardege, J., Hird, C., Hsieh, Y.-W., Hui, J., Mutemi, K. N., Schneider, S. Q., Simakov, O., Vergara, H. M., Vervoort, H., Jekley, G., Tessmar-Raible, K., Raible, F., Arendt, D. The Nereid on the rise: Platynereis as a model system. EvoDevo, 12(1), (2021): 10, https://doi.org/10.1186/s13227-021-00180-3.

Description: The Nereid Platynereis dumerilii (Audouin and Milne Edwards (Annales des Sciences Naturelles 1:195–269, 1833) is a marine annelid that belongs to the Nereididae, a family of errant polychaete worms. The Nereid shows a pelago-benthic life cycle: as a general characteristic for the superphylum of Lophotrochozoa/Spiralia, it has spirally cleaving embryos developing into swimming trochophore larvae. The larvae then metamorphose into benthic worms living in self-spun tubes on macroalgae. Platynereis is used as a model for genetics, regeneration, reproduction biology, development, evolution, chronobiology, neurobiology, ecology, ecotoxicology, and most recently also for connectomics and single-cell genomics. Research on the Nereid started with studies on eye development and spiralian embryogenesis in the nineteenth and early twentieth centuries. Transitioning into the molecular era, Platynereis research focused on posterior growth and regeneration, neuroendocrinology, circadian and lunar cycles, fertilization, and oocyte maturation. Other work covered segmentation, photoreceptors and other sensory cells, nephridia, and population dynamics. Most recently, the unique advantages of the Nereid young worm for whole-body volume electron microscopy and single-cell sequencing became apparent, enabling the tracing of all neurons in its rope-ladder-like central nervous system, and the construction of multimodal cellular atlases. Here, we provide an overview of current topics and methodologies for P. dumerilii, with the aim of stimulating further interest into our unique model and expanding the active and vibrant Platynereis community.

Description: Funding resources are shown after author initials. EAW: BBSRC David Phillips Fellowship BB/T00990X/1. BDÖ: NIH NIGMS MIRA 1R35GM138008-01; NSF-EDGE Award no 1923429; Hibbitt Startup Funds. GJ, LABC, CH: Wellcome Trust Investigator Award 214337/Z/18/Z. KNM: Marie Sklodowska-Curie fellow supported by the European Union’s Horizon 2020 research and innovation programme under grant agreement No. 766053, project EvoCELL. NR: European Union Horizon 2020, Marie Skłodowska-Curie Grant No 838225. MCG: Stazione Zoologica A. Dohrn (Napoli) and the Ischia Marine Center technical staff; Open University PhD programme; ASSEMBLE; PON-MODO project (Campania Region, Italy), RITMARE - Flag project, Italy; MARES Consortium. Thanks to the ECCSEL - NatLab Italy facilities, managed by the OGS (Trieste), to support collection at Panarea and Vulcano islands. JDH: NERC award NE/T001577/1. MHT: Deutsche Forschungsgemeinschaft (DFG), Grant Number TO563/7-1. EG and MV: Labex ‘Who Am I?’ (No. ANR-11-LABX-0071) funded by the French Government through its ‘Investments for the Future’ program operated by the ANR under Grant No. ANR-11-IDEX-0005-01, Centre National de la Recherche Scientifique (DBM Grant), Université de Paris (IDEX Emergence grant 2020), Agence Nationale de la Recherche (Grant TELOBLAST no. ANR-16-CE91-0007; Grant STEM No. ANR-19-CE27-0027-02), the «Association pour la Recherche sur le Cancer» (Grant PJA 20191209482), and the «Ligue Nationale Contre le Cancer» (Grant RS20/75-20). SQS: NSF (US) Award IOS-1455185, MOST (TW) 108-2311-B-001-002-MY3, Academia Sinica Career Development Award AS-CDA-110-L02, and the Institute of Cellular and Organismic Biology (ICOB) of Academia Sinica (TW). YWH: Deutsche Forschungsgemeinschaft (DFG), grant number TO563/7-1 (to Pavel Tomancak). OS: Austrian Science Fund Grant P32190. GB: The Balavoine Lab was funded by the CNRS, the Université de Paris and grants from the ANR (TELOBLAST no. ANR-16-CE91-0007) and from the ARC (PJA 20181208248). FR and KTR: The research leading to these results has received funding from the European Research Council under the European Community’s Seventh Framework Programme (FP7/2007–2013)/ERC Grant Agreement 260304 (F.R.) and ERC Grant Agreement 337011 (K.T.-R.); the Horizon 2020 Programme ERC Grant Agreement 81995 (K.T.-R.); the research platforms ‘Rhythms of Life’ (K.T.-R., F.R.) and “Single-cell genomics of stem cells” (F.R.) of the University of Vienna; the Austrian Science Fund (FWF) START award, project Y413 (K.T.-R.); the Austrian Science Fund (FWF) projects P28970 (K.T.-R.) and I2972 (F.R.); the Austrian Science Fund (FWF) grant F78 (K.T.-R., F.R.). DA and PB ERC Advanced grant NeuralCellTypeEvo #788921.

Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Özpolat, B. D., Randel, N., Williams, E. A., Bezares-Calderón, L. A., Andreatta, G., Balavoine, G., Bertucci, P. Y., Ferrier, D. E. K., Gambi, M. C., Gazave, E., Handberg-Thorsager, M., Hardege, J., Hird, C., Hsieh, Y.-W., Hui, J., Mutemi, K. N., Schneider, S. Q., Simakov, O., Vergara, H. M., Jékely, G., Tessmar-Raible, K., Raible, F., Arendt, D. The Nereid on the rise: Platynereis as a model system. EvoDevo, 12(1), (2021): 10, https://doi.org/10.1186/s13227-021-00180-3.

Description: The Nereid Platynereis dumerilii (Audouin and Milne Edwards (Annales des Sciences Naturelles 1:195–269, 1833) is a marine annelid that belongs to the Nereididae, a family of errant polychaete worms. The Nereid shows a pelago-benthic life cycle: as a general characteristic for the superphylum of Lophotrochozoa/Spiralia, it has spirally cleaving embryos developing into swimming trochophore larvae. The larvae then metamorphose into benthic worms living in self-spun tubes on macroalgae. Platynereis is used as a model for genetics, regeneration, reproduction biology, development, evolution, chronobiology, neurobiology, ecology, ecotoxicology, and most recently also for connectomics and single-cell genomics. Research on the Nereid started with studies on eye development and spiralian embryogenesis in the nineteenth and early twentieth centuries. Transitioning into the molecular era, Platynereis research focused on posterior growth and regeneration, neuroendocrinology, circadian and lunar cycles, fertilization, and oocyte maturation. Other work covered segmentation, photoreceptors and other sensory cells, nephridia, and population dynamics. Most recently, the unique advantages of the Nereid young worm for whole-body volume electron microscopy and single-cell sequencing became apparent, enabling the tracing of all neurons in its rope-ladder-like central nervous system, and the construction of multimodal cellular atlases. Here, we provide an overview of current topics and methodologies for P. dumerilii, with the aim of stimulating further interest into our unique model and expanding the active and vibrant Platynereis community.

Description: Funding resources are shown after author initials. EAW: BBSRC David Phillips Fellowship BB/T00990X/1. BDÖ: NIH NIGMS MIRA 1R35GM138008-01; NSF-EDGE Award no 1923429; Hibbitt Startup Funds. GJ, LABC, CH: Wellcome Trust Investigator Award 214337/Z/18/Z. KNM: Marie Sklodowska-Curie fellow supported by the European Union’s Horizon 2020 research and innovation programme under grant agreement No. 766053, project EvoCELL. NR: European Union Horizon 2020, Marie Skłodowska-Curie Grant No 838225. MCG: Stazione Zoologica A. Dohrn (Napoli) and the Ischia Marine Center technical staff; Open University PhD programme; ASSEMBLE; PON-MODO project (Campania Region, Italy), RITMARE - Flag project, Italy; MARES Consortium. Thanks to the ECCSEL - NatLab Italy facilities, managed by the OGS (Trieste), to support collection at Panarea and Vulcano islands. JDH: NERC award NE/T001577/1. MHT: Deutsche Forschungsgemeinschaft (DFG), Grant Number TO563/7-1. EG and MV: Labex ‘Who Am I?’ (No. ANR-11-LABX-0071) funded by the French Government through its ‘Investments for the Future’ program operated by the ANR under Grant No. ANR-11-IDEX-0005-01, Centre National de la Recherche Scientifique (DBM Grant), Université de Paris (IDEX Emergence grant 2020), Agence Nationale de la Recherche (Grant TELOBLAST no. ANR-16-CE91-0007; Grant STEM No. ANR-19-CE27-0027-02), the «Association pour la Recherche sur le Cancer» (Grant PJA 20191209482), and the «Ligue Nationale Contre le Cancer» (Grant RS20/75-20). SQS: NSF (US) Award IOS-1455185, MOST (TW) 108-2311-B-001-002-MY3, Academia Sinica Career Development Award AS-CDA-110-L02, and the Institute of Cellular and Organismic Biology (ICOB) of Academia Sinica (TW). YWH: Deutsche Forschungsgemeinschaft (DFG), grant number TO563/7-1 (to Pavel Tomancak). OS: Austrian Science Fund Grant P32190. GB: The Balavoine Lab was funded by the CNRS, the Université de Paris and grants from the ANR (TELOBLAST no. ANR-16-CE91-0007) and from the ARC (PJA 20181208248). FR and KTR: The research leading to these results has received funding from the European Research Council under the European Community’s Seventh Framework Programme (FP7/2007–2013)/ERC Grant Agreement 260304 (F.R.) and ERC Grant Agreement 337011 (K.T.-R.); the Horizon 2020 Programme ERC Grant Agreement 81995 (K.T.-R.); the research platforms ‘Rhythms of Life’ (K.T.-R., F.R.) and “Single-cell genomics of stem cells” (F.R.) of the University of Vienna; the Austrian Science Fund (FWF) START award, project Y413 (K.T.-R.); the Austrian Science Fund (FWF) projects P28970 (K.T.-R.) and I2972 (F.R.); the Austrian Science Fund (FWF) grant F78 (K.T.-R., F.R.). DA and PB ERC Advanced grant NeuralCellTypeEvo #788921.

Description: © The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in eLife 6 (2017): e30463, doi:10.7554/eLife.30463.

Description: Cell lineage, cell cycle, and cell fate are tightly associated in developmental processes, but in vivo studies at single-cell resolution showing the intricacies of these associations are rare due to technical limitations. In this study on the marine annelid Platynereis dumerilii, we investigated the lineage of the 4d micromere, using high-resolution long-term live imaging complemented with a live-cell cycle reporter. 4d is the origin of mesodermal lineages and the germline in many spiralians. We traced lineages at single-cell resolution within 4d and demonstrate that embryonic segmental mesoderm forms via teloblastic divisions, as in clitellate annelids. We also identified the precise cellular origins of the larval mesodermal posterior growth zone. We found that differentially-fated progeny of 4d (germline, segmental mesoderm, growth zone) display significantly different cell cycling. This work has evolutionary implications, sets up the foundation for functional studies in annelid stem cells, and presents newly established techniques for live imaging marine embryos.

Description: Labex (No.ANR-11-LABX-0071); Agence Nationale de la Recherche (METAMERE no. ANR-12-BSV2-0021); Agence Nationale de la Recherche (TELOBLAST no. ANR-16-CE91-0007)