Abstract
Transitions in gene regulatory processes responsible for the emergence of specialized cell types and spatiotemporal regulation of developmental signaling prior to the divergence of Cnidaria and Bilateria are poorly understood. As a sister group of Bilateria, the phylum Cnidaria can provide significant insights into these processes. Among the cnidarians, hydrae have been studied for >250 years to comprehend the mechanisms underlying their unique immortality and robust regenerative capacity. Studies on Hydra spp. and other pre-bilaterians alike have advanced our understanding of the evolutionary underpinnings governing eumetazoan tissue development, homeostasis, and regeneration. In addition to its regenerative potential, Hydra exhibits continuously active axial patterning due to its peculiar tissue dynamics. These distinctive physiological processes necessitate large scale gene expression changes that are governed by the multitude of epigenetic mechanisms operating in cells. This review highlights the contemporary knowledge of epigenetic regulation in Hydra with contemporary studies from other members of Cnidaria, as well as the interplay between regulatory mechanisms wherever demonstrated. The studies covered in the scope of this review reveal both ancestral and divergent roles played by conserved epigenetic mechanisms with emphasis on transcriptional regulation. Additionally, single-cell transcriptomics data was mined to predict the physiological relevance of putative gene regulatory components, which is in agreement with published findings and yielded insights into the possible functions of the gene regulatory mechanisms that are yet to be deciphered in Hydra, such as DNA methylation. Finally, we delineate potentially rewarding epigenetics research avenues that can further leverage the unique biology of Hydra.
Highlights
Epigenetic RegulationCells are the fundamental unit of life
Siebert et al recently performed scRNA-seq on Hydra vulgaris AEP by dissociating polyps and individually sequencing ∼25,000 cells, thereby generating an atlas of gene expression across the constituent cell types in their various molecular “states.” Analysis of the dataset confirmed previous results, such as the head organizer-specific expression of wnt3a and the graded downregulation of dickkopflike 1/2/4 C during the transdifferentiation of zymogen gland cells to granular mucous gland cells (Siebert et al, 2019). We have mined this dataset for the expression levels of confirmed and predicted orthologs of epigenetic regulators in Hydra, and the cell types found to have the different levels of expression of each ortholog were noted
This study found that Hydra Yin Yang 1 (YY1) directly interacts with Polycomb Repressive Complex 2 (PRC2), raising the possibility that Hydra YY1 may play an evolutionarily conserved role in PRC2 recruitment for targeted gene repression
Summary
Cells are the fundamental unit of life. Cell fate and function are determined by the biomolecular complement at homeostasis, which is responsive to the internal and external stimuli. Many types of histone modifications have been associated with transcriptional regulation, the well-studied modifications include the methylation and acetylation of specific lysine residues predominantly on H3 and H4 with many known roles in transcriptional regulation and cell fate determination. Methylation of lysines on histones does not have a universally activating or repressive function and has a greater level of specificity both in the role of the modification and the proteins that regulate the modifications. Each type of histone modification has been ascribed a specific role, it is the combinatorial occurrence of the marks that determines the status of transcription in cells (Wang et al, 2008) Bivalent nucleosomes have both activating (H3K4me3) and repressive (H3K27me3) histone marks and transcriptionally poised chromatin (Bernstein et al, 2006).
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