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Systemic coordination of whole-body tissue remodeling during local regeneration in sea anemones

ABSTRACT: The complexity of regeneration extends beyond local wound responses, eliciting systemic processes engaging the entire organism. However, their functional relevance, and the spatial and temporal orchestration of the underlying molecular processes distant from the injury site remain unknown. Here, we demonstrate that local regeneration in the cnidarian Nematostella vectensis involves a systemic homeostatic response, leading to coordinated whole-body remodeling. Leveraging spatial transcriptomics, endogenous protein tagging, and live imaging, we comprehensively dissect this systemic response at the organismal scale. We identify proteolysis as critical process driven by both local and systemic upregulation of metalloproteases. We show that metalloproteinase expression levels and activity scale with the extent of tissue loss, leading to proportional long-range movement of tissue and its associated extracellular matrix. Our findings demonstrate the adaptive nature of the systematic response in regeneration. We propose that this integrated regenerative mechanism enables the organism to maintain shape homeostasis while coping with injuries.

ORGANISM(S): Nematostella vectensis

PROVIDER: GSE271567 | GEO | 2024/10/21

REPOSITORIES: GEO

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Project description:We utilized the Nematostella vectensis to quantify gene expression differences and loss during light:dark cycling and immediately after light cue removal through comparisons of 136 transcriptomes Organismal responses to light:dark cycles can result from two general processes: (i) direct response to light or (ii) a free-running rhythm (i.e., a circadian clock). Previous research in cnidarians has shown that candidate circadian clock genes have rhythmic expression in the presence of diel lighting, but these oscillations appear to be lost quickly after removal of the light cue. Here, we measure whole-organism gene expression changes in 136 transcriptomes of the sea anemone Nematostella vectensis, entrained to a light:dark environment and immediately following light cue removal to distinguish two broadly defined responses in cnidarians: light entrainment and circadian regulation. Direct light exposure resulted in significant differences in expression for hundreds of genes, including more than 200 genes with rhythmic, 24-hour periodicity. Removal of the lighting cue resulted in the loss of significant expression for 80% of these genes after one day, including most of the hypothesized cnidarian circadian genes. Further, 70% of these candidate genes were phase shifted. Most surprisingly, thousands of genes, some of which are involved in oxidative stress, DNA damage response, and chromatin modification, had significant differences in expression in the 24 hours following light removal, suggesting that loss of the entraining cue may induce a cellular stress response. Together, our findings suggest that a majority of genes with significant differences in expression for anemones cultured under diel lighting are largely driven by the primary photoresponse rather than a circadian clock when measured at the whole animal level. These results provide context for the evolution of cnidarian circadian biology and help to disassociate two commonly confounded factors driving oscillating phenotypes.

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Systemic coordination of whole-body tissue remodeling during local regeneration in sea anemones

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