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Integrative analysis of Hydra head regeneration reveals activation of distal enhancer-like elements [RNA-seq]

ABSTRACT: The cnidarian model organism Hydra has long been studied for its remarkable ability to regenerate its head, which is controlled by a head organizer located near the hypostome. Cnidarians and bilaterians diverged about 600 millions years ago but the gene contents of species of both phyla are surprisingly similar despite divergent morphologies and functions. While little is known about the role of cis-regulatory elements in cnidarians, understanding gene regulatory mechanisms in cnidarians can potentially shed light on metazoan evolution. The canonical Wnt pathway plays a central role in head organizer function during regeneration and during bud formation, which is the asexual mode of reproduction in Hydra. However, it is unclear how shared the developmental programs of head organizer genesis are in budding and regeneration. Time-series analysis of gene expression changes during head regeneration and budding revealed a set of 298 differentially expressed genes during the 48-hour head regeneration and 72-hour budding time-courses. In order to understand the regulatory elements controlling hydra head regeneration, we first identified 27,137 open-chromatin elements that are open in one or more sections of organism. We used histone modification ChIP-seq to identify 9998 candidate proximal promoter and 3018 candidate enhancer-like regions respectively. We show that a subset of these regulatory elements is dynamically remodeled during head regeneration and identify a set of transcription factor motifs that are enriched in the enhancer regions activated during head regeneration. Our results show that Hydra displays complex gene regulatory structures of developmentally dynamic enhancers, which suggests that the evolution of complex developmental enhancers predates the split of cnidarians and bilaterians.

ORGANISM(S): Hydra vulgaris

PROVIDER: GSE127279 | GEO | 2019/12/31

REPOSITORIES: GEO

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Project description:Animals capable of whole-body regeneration can fully restore any tissue lost due to injury. Because different types of injury may require the regeneration of different structures, transcription during whole-body regeneration needs to dynamically adapt to meet the requirements specific to any given injury. However, the regulatory mechanisms responsible for modulating the transcriptional response to injury are poorly understood at the molecular level. We therefore used the highly regenerative cnidarian polyp, Hydra vulgaris, to better understand how transcription in wounded tissue responds to its surrounding tissue environment to enable the restoration of the original body plan. We comprehensively characterized changes in transcript abundance and chromatin accessibility during two types of regeneration, oral and aboral regeneration, and found that the initial transcriptional response to injury was the same regardless of the injury’s tissue environment. This initial response included the activation of the canonical Wnt signaling pathway, which specifies oral tissue in cnidarians, likely through the direct upregulation of Wnt ligands by conserved injury responsive bZIP transcription factors. The duration of the injury-induced increase in Wnt signaling depended on the injury’s tissue context, as Wnt signaling was activated only transiently during aboral regeneration but showed sustained activation during oral regeneration. Inhibiting TCF, the transcription factor downstream of canonical Wnt signaling, delayed the onset of oral- and aboral-specific transcription genome-wide, suggesting that proper regulation of canonical Wnt signaling is critical for both types of regeneration. Finally, we found that Wnt signaling was also activated by puncture wounds, and that removing pre-existing organizers induced these injuries to undergo ectopic head regeneration. These findings suggest that head regeneration is the default response to injury in Hydra, and that other wound repair outcomes are the result of inhibitory signals produced by the surrounding tissue environment. Furthermore, our work raises the possibility that Wnt signaling may be part of an ancient and conserved wound response program that predates the split of bilaterians and cnidarians over 500 million years ago.

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Integrative analysis of Hydra head regeneration reveals activation of distal enhancer-like elements [RNA-seq]

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