[en] Species within nearly all extant animal lineages are capable of regenerating body parts. However, it remains unclear whether the gene expression programme controlling regeneration is evolutionarily conserved. Brittle stars are a species-rich class of echinoderms with outstanding regenerative abilities, but investigations into the genetic bases of regeneration in this group have been hindered by the limited genomic resources. Here we report a chromosome-scale genome assembly for the brittle star Amphiura filiformis. We show that the brittle star genome is the most rearranged among echinoderms sequenced so far, featuring a reorganized Hox cluster reminiscent of the rearrangements observed in sea urchins. In addition, we performed an extensive profiling of gene expression during brittle star adult arm regeneration and identified sequential waves of gene expression governing wound healing, proliferation and differentiation. We conducted comparative transcriptomic analyses with other invertebrate and vertebrate models for appendage regeneration and uncovered hundreds of genes with conserved expression dynamics, particularly during the proliferative phase of regeneration. Our findings emphasize the crucial importance of echinoderms to detect long-range expression conservation between vertebrates and classical invertebrate regeneration model systems.
Disciplines :
Zoology
Author, co-author :
Parey, Elise ; Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, London, UK. e.parey@ucl.ac.uk
Ortega-Martinez, Olga ; Tjärnö Marine Laboratory, Department of Marine Sciences, University of Gothenburg, Strömstad, Sweden
DELROISSE, Jérôme ; Université de Mons - UMONS > Faculté des Sciences > Service de Biologie des Organismes Marins et Biomimétisme
Piovani, Laura ; Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, London, UK
Czarkwiani, Anna ; Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, London, UK ; Technische Universität Dresden, Center for Regenerative Therapies Dresden (CRTD), Dresden, Germany
Dylus, David ; Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, London, UK ; Roche Pharmaceutical Research and Early Development (pRED), Cardiovascular and Metabolism, Immunology, Infectious Disease, and Ophthalmology (CMI2O), F. Hoffmann-La Roche Ltd, Basel, Switzerland
Arya, Srishti ; Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, London, UK ; MRC Laboratory of Medical Sciences, Imperial College London, London, UK
Dupont, Samuel; Department of Biology and Environmental Science, University of Gothenburg, Kristineberg Marine Research Station, Fiskebäckskil, Sweden ; IAEA Marine Environment Laboratories, Radioecology Laboratory, Quai Antoine 1er, Monaco
Thorndyke, Michael; Department of Biology and Environmental Science, University of Gothenburg, Kristineberg Marine Research Station, Fiskebäckskil, Sweden
Larsson, Tomas; Department of Cell and Molecular Biology, National Bioinformatics Infrastructure Sweden, Science for Life Laboratory, Uppsala University, Uppsala, Sweden
Johannesson, Kerstin ; Tjärnö Marine Laboratory, Department of Marine Sciences, University of Gothenburg, Strömstad, Sweden
Buckley, Katherine M ; Department of Biological Sciences, Auburn University, Auburn, AL, USA
Martinez, Pedro ; Departament de Genètica, Microbiologia, i Estadística, Universitat de Barcelona, Barcelona, Spain ; Institut Català de Recerca i Estudis Avançats (ICREA), Barcelona, Spain
Oliveri, Paola ; Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, London, UK. p.oliveri@ucl.ac.uk
Marlétaz, Ferdinand ; Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, London, UK. f.marletaz@ucl.ac.uk
S864 - Biologie des Organismes Marins et Biomimétisme
Research institute :
Research Institute for Biosciences
Funders :
Royal Society RCUK | Biotechnology and Biological Sciences Research Council Leverhulme Trust Japan Society for the Promotion of Science London Vetenskapsrådet Fonds De La Recherche Scientifique - FNRS National Science Foundation EC | Horizon 2020 Framework Programme EC | EC Seventh Framework Programm | FP7 Research infrastructures
Funding text :
This work was supported by the Centre for Marine Evolutionary Biology at the University of Gothenburg ( http://www.cemeb.science.gu.se/ ) and the IMAGO project led by Anders Blomberg. E.P. was supported by a Newton International Fellowship from the Royal Society (NIF\\R1\\222125). F.M. was supported by a Royal Society University Research Fellowship (URF\\R1\\191161) and a Japan Society for the Promotion of Science Kakenhi grant (JP 19K06620). L.P. was supported by the Leverhulme Trust Research Project (grant number RPG-2021-436 to F.M. supporting L.P.) and the BBSRC (grant BB/V01109X/1 to F.M. supporting L.P.). O.O.-M. was financially supported by CEMEB through grants from Swedish research councils Formas and VR (217-2008-1719) and from a VR grant to K.J. (253016979). J.D. was supported by an F.R.S.-FNRS research project (PDR, 40013965), previously held an F.R.S.-FNRS \u2018Charg\u00E9 de recherche\u2019 fellowship (CR, 34761044), and also received financial support from an F.R.S.-FNRS research project (PDR, T.0169.20) and the Biosciences Research Institute of the University of Mons. P.M. visited the Department of Genetics, Evolution and Environment of UCL financed by a short-term scientific mission Grant of the EU COST Action MARISTEM (CA-16203). K.M.B. was supported by the National Science Foundation (NSF Award 2131297). P.O. visits to the Kristineberg Marine Station (Sweden) were supported by the KVA fund SL2015-0048 from the Royal Swedish Academy of Sciences and the EU FP7 Research Infrastructures Initiative ASSEMBLE (227799). P.O. was supported by the BBSRC (BB/W017865/1). The IAEA thanks the Government of the Principality of Monaco for the support provided to its Marine Environment Laboratories. We thank the staff at the Kristineberg Center for Marine Research and Innovation, especially U. Schwarz, for assistance during animal collection; A. Sabar\u00ED i Mart\u00ED, E. Onal, L. Henke and W. Hart for assistance in conducting experiments. We acknowledge the Okinawa Institute of Science and Technology sequencing facility and its members for support, especially N. Arakaki and M. Kawamitsu. Finally, we thank J. Rast for helpful comments on the manuscript. The authors dedicate this manuscript to Michael Thorndyke and R. Andrew Cameron, who were both instrumental in the early stages of this project but, sadly, passed away before analyses were completed. Without their contributions, this work would not have been possible.
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