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FGF signalling plays similar roles in development and regeneration of the skeleton in the brittle star Amphiura filiformis.

ABSTRACT: Regeneration as an adult developmental process is in many aspects similar to embryonic development. Although many studies point out similarities and differences, no large-scale, direct and functional comparative analyses between development and regeneration of a specific cell type or structure in one animal exist. Here, we use the brittle star Amphiura filiformis to characterise the role of the FGF signalling pathway during skeletal development in embryos and arm regeneration. In both processes, we find ligands expressed in ectodermal cells that flank underlying skeletal mesenchymal cells, which express the receptors. Perturbation of FGF signalling showed inhibited skeleton formation in both embryogenesis and regeneration, without affecting other key developmental processes. Differential transcriptome analysis finds mostly differentiation genes rather than transcription factors to be downregulated in both contexts. Moreover, comparative gene analysis allowed us to discover brittle star-specific differentiation genes. In conclusion, our results show that the FGF pathway is crucial for skeletogenesis in the brittle star, as in other deuterostomes, and provide evidence for the re-deployment of a developmental gene regulatory module during regeneration.

SUBMITTER: Czarkwiani A

PROVIDER: S-EPMC8180256 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The brittle star Amphiura filiformis, which regenerates its arms post autotomy, is emerging as a useful model for studying the molecular underpinnings of regeneration, aided by the recent availability of some molecular resources. During regeneration a blastema initially is formed distally to the amputation site, and then a rapid rebuild is obtained by adding metameric units, which will eventually differentiate and become fully functional. In this work we first characterize the developmental process of the regenerating arms using two differentiation markers for muscle and skeletal structures - Afi-trop-1 and Afi-?coll. Both genes are not expressed in the blastema and newly added undifferentiated metameric units. Their expression at different regenerating stages shows an early segregation of muscle and skeletal cells during the regenerating process, long before the metameric units become functional. We then studied the expression of a set of genes orthologous of the sea urchin transcription factors involved in the development of skeletal and non-skeletal mesoderm: Afi-ets1/2, Afi-alx1, Afi-tbr, Afi-foxB and Afi-gataC. We found that Afi-ets1/2, Afi-alx1, Afi-foxB and Afi-gataC are all expressed at the blastemal stage. As regeneration progresses those genes are expressed in a similar small undifferentiated domain beneath the distal growth cap, while in more advanced metameric units they become restricted to different skeletal domains. Afi-foxB becomes expressed in non-skeletal structures. This suggests that they might play a combinatorial role only in the early cell specification process and that subsequently they function independently in the differentiation of different structures. Afi-tbr is not present in the adult arm tissue at any stage of regeneration. In situ hybridization results have been confirmed with a new strategy for quantitative PCR (QPCR), using a subdivision of the three stages of regeneration into proximal (differentiated) and distal (undifferentiated) arm segments.

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FGF signalling plays similar roles in development and regeneration of the skeleton in the brittle star Amphiura filiformis.

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