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The Rapid Regenerative Response of a Model Sea Anemone Species Exaiptasia pallida Is Characterised by Tissue Plasticity and Highly Coordinated Cell Communication

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Abstract

Regeneration of a limb or tissue can be achieved through multiple different pathways and mechanisms. The sea anemone Exaiptasia pallida has been observed to have excellent regenerative proficiency, but this has not yet been described transcriptionally. In this study, we examined the genetic expression changes during a regenerative timecourse and reported key genes involved in regeneration and wound healing. We found that the major response was an early (within the first 8 h) upregulation of genes involved in cellular movement and cell communication, which likely contribute to a high level of tissue plasticity resulting in the rapid regeneration response observed in this species. We find the immune system was only transcriptionally active in the first 8 h post-amputation and conclude, in accordance with previous literature, that the immune system and regeneration have an inverse relationship. Fifty-nine genes (3.8% of total) differentially expressed during regeneration were identified as having no orthologues in other species, indicating that regeneration in E. pallida may rely on the activation of species-specific novel genes. Additionally, taxonomically restricted novel genes, including species-specific novels, and highly conserved genes were identified throughout the regenerative timecourse, showing that both may work in concert to achieve complete regeneration.

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Data Availability Statement

Raw reads for the Exaiptasia pallida regeneration timecourse are available on the Sequence Read Archive (SRA, NCBI) under BioProject accession number PRJNA507308. Full list of BioSample accession numbers are in Supplementary Table S1. Select gene annotation data is available in the supplementary data, additional gene annotations and read mapping files can be provided upon request. Reads for transcriptomes assembled locally and used in OrthoFinder analysis are on the SRA (accession details are provided in literature as cited) but assembled transcriptome files and annotations can be provided upon request. Raw reads for the three sea anemone transcriptomes generated here (Diadumene lineata, Stichodactyla mertensii and Triactis producta) can be found under BioProject accession number PRJNA507679.

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Acknowledgements

Computational resources used in this work were provided by the HPC (High Performance Computing). Lab space was provided by MGRF (Molecular Genomics Research Facility) and technical support was provided by Vincent Chand and Sahana Manoli at MGRF at Queensland University of Technology, Brisbane, Australia. The authors would like to thank the members of the Prentis lab group, in particular Jessica O’Callaghan, for their insights and support. The authors would also like to thank the marine lab crew at QUT for their continual help with care and maintenance of the marine animals. Special thanks goes to Dr. Libby Liggins (Massey University, New Zealand) for providing the D. lineata sample.

Funding

The authors would like to acknowledge the Institute of Health and Biomedical Innovation (IHBI) for providing funding for the generation of raw reads for this project.

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Contributions

C.V.D.B., A.P., J.S. and P.P. conceived and designed the research; C.V.D.B., J.S. and H.S. performed the experiments; C.V.D.B and H.S. sequenced and assembled the transcriptomes; C.V.D.B analysed the data; C.V.D.B., A.P., E.G., E.P., J.S., T.W. and P.P. interpreted the results of experiments; C.V.D.B. prepared the figures; C.V.D.B. and P.P. drafted the manuscript; and C.V.D.B., A.P., E.G., E.P., J.S., H.S., T.W. and P.P. edited, revised and approved the final version of the manuscript.

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Correspondence to Chloé A. van der Burg.

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This project did not require animal ethics approval. Sample collection for sea anemones collected in Australia (all sea anemone datasets generated here, except for Diadumene lineata) was authorised under the Fisheries Act 1994 (General Fisheries Permit), permit number: 166312. Sample collection for Diadumene lineata, which was collected in New Zealand, was authorised under the Ministry for Primary Industries Special Permit (632).

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van der Burg, C.A., Pavasovic, A., Gilding, E.K. et al. The Rapid Regenerative Response of a Model Sea Anemone Species Exaiptasia pallida Is Characterised by Tissue Plasticity and Highly Coordinated Cell Communication. Mar Biotechnol 22, 285–307 (2020). https://doi.org/10.1007/s10126-020-09951-w

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