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Biology subjects

Warner, J. F.

Publications and source records attributed to Warner, J. F..

4 recordsLinked to original sources

Extreme conservation of cnidarian stinging cell identity despite 600 million years of evolution

Understanding how cells specialize is essential for reconstructing the diversification of life on earth. Cnidocytes (stinging cells) have a single origin in the stem cnidarian ([~]800mya) and have since specialized into extremes in morphology and function. Using single-cell RNA sequencing and transcriptional lineage reconstruction in a coral and a sea anemone, we show that a single gene (FoxL2) controls a critical switch point in the evolution of cnidocyte diversity: the decision to be a piercing cell (nematocyte) or an ensnaring cell (spirocyte). Nematocytes are lowly conserved between species and express younger genes, reflecting the continued diversification of this cell lineage. Surprisingly, ensnaring cells are one of the most highly conserved differentiated cell types and express older genes than nematocytes. This suggests spirocytes reached an adaptive peak early and have changed little during the 600 million years since corals and sea anemones last shared a common ancestor, making them living fossil cells.

evolutionary biology↗

Evolutionary rewiring of the endomesoderm gene regulatory networks specify skeleton secreting cells in stony corals.

Stony corals are the eponymous keystone organisms for the most diverse marine ecosystems on earth: coral reefs. Despite their importance, little is known about the developmental genetic programs that drive their embryonic development and subsequent emergence of coral-specific traits. Like all developmental processes, coral development is governed by a series of genetic interactions collectively termed a gene regulatory network. Evolutionary changes in these gene regulatory networks are key sources of biological innovation, but how these networks operate in corals and how they have changed over time remains poorly understood. Here, we integrate chromatin profiling and transcriptomics to define the cis-regulatory architecture of early development in stony corals using the emerging model, Astrangia poculata. We find that key elements of the deeply conserved cnidarian endomesoderm gene regulatory network have been co-opted into a novel subnetwork that specifies secretory cells in corals. Using transgenic reporter assays, we found that a proximal cis-regulatory element of the endomesodermal gene Brachyury is sufficient to drive coral-specific expression patterns in the sea anemone Nematostella vectensis, demonstrating these elements as a key evolvable unit in stony corals. Collectively these findings establish a gene-regulatory framework for coral development and cell specification and suggest that evolutionary rewiring of ancestral developmental programs is a key driver in the evolution and diversification of stony corals.

developmental biology↗

Microinjection, gene knockdown, and CRISPR-mediated gene knock-in in the hard coral, Astrangia poculata

Cnidarians have become valuable models for understanding many aspects of developmental biology including the evolution of body plan diversity, novel cell type specification, and regeneration. Most of our understanding of gene function during early development in cnidarians comes from a small number of experimental systems including the sea anemone, Nematostella vectensis. Few molecular tools have been developed for use in hard corals, limiting our understanding of this diverse and ecologically important clade. Here, we report the development of a suite of tools for manipulating and analyzing gene expression during early development in the northern star coral, Astrangia poculata. We present methods for gene knockdown using short hairpin RNAs, gene overexpression using exogenous mRNAs, and endogenous gene tagging using CRISPR-mediated gene knock-in. Combined with our ability to control spawning in the laboratory, these tools make A. poculata a tractable experimental system for investigative studies of coral development. Further application of these tools will enable functional analyses of embryonic patterning and morphogenesis across Anthozoa and open new frontiers in coral biology research. Summary StatementThis study reports the development of the first transgenic knock-in coral, providing the opportunity to track the behavior of various cell types during early coral development.

developmental biology↗

Regeneration is a partial redeployment of the embryonic gene network

For over a century, researchers have been trying to understand the relationship between embryogenesis and regeneration. A long-standing hypothesis is that biological processes implicated in embryonic development are re-deployed during regeneration. In the past decade, we have begun to understand the relationships of genes and their organization into gene regulatory networks (GRN) driving embryonic development and regeneration in diverse taxa. Here, we compare embryonic and regeneration GRNs in the same species to investigate how regeneration re-uses genetic interactions originally set aside for embryonic development. Using a well-suited embryonic development and whole-body regeneration model, the sea anemone Nematostella vectensis, we show that at the transcriptomic level the regenerative program partially re-uses elements of the embryonic gene network along with a small cohort of genes that are specifically activated during the process of regeneration. We further identified co-expression modules that are either i) highly conserved between these two developmental trajectories and involved in core biological processes (e.g., terminal differentiation) or ii) regeneration specific modules that drive cellular events, such as apoptosis, that are unique to regeneration. Our global transcriptomic approach suggested that regeneration reactivates embryonic gene modules following regeneration-specific network logic. We thus verified this observation by functionally dissecting the role of MEK/ERK signaling during regeneration and established a first blueprint of the regeneration MEK/ERK-dependent GRN in Nematostella. Comparing the latter to the existing GRN underlying embryogenic development of the same species, we show at the network level that i) regeneration is a partial redeployment of the embryonic GRN, ii) embryonic gene modules are rewired during regeneration and iii) they are interconnected to novel down-stream targets, including "regeneration-specific" genes. Significance statementIn this intra-species transcriptomic comparison of embryonic development and regeneration in a whole-body regeneration model, the sea anemone Nematostella vectensis, we identified that 1) regeneration is a transcriptionally modest event compared to embryonic development and 2) that although regeneration re-uses embryonic genetic interactions, it does so by using regeneration specific network logic. In addition to identifying that apoptosis is a regeneration-specific event in Nematostella, this study reveals that GRN modules are reshuffled from one developmental trajectory to the other, even when accomplishing the same task (e.g. forming a fully functional organism). These findings highlight the plasticity of network architecture and set the basis for determining and functionally dissecting regeneration-inducing regulatory elements. From an evolutionary perspective, our study sets the foundation for further comparative work and provides new opportunities to understand why certain organisms can regenerate while others cannot.

developmental biology↗