The brittle star genome illuminates the genetic basis of animal appendage regeneration

Author:

Parey EliseORCID,Ortega-Martinez OlgaORCID,Delroisse JérômeORCID,Piovani LauraORCID,Czarkwiani AnnaORCID,Dylus DavidORCID,Arya SrishtiORCID,Dupont Samuel,Thorndyke Michael,Larsson Tomas,Johannesson KerstinORCID,Buckley Katherine M.ORCID,Martinez PedroORCID,Oliveri PaolaORCID,Marlétaz FerdinandORCID

Abstract

AbstractSpecies 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.

Funder

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

Publisher

Springer Science and Business Media LLC

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