2024 |
Alexandra M Vargas, Melissa B DeBiasse, Lana L Dykes, Allison Edgar, T Danielle Hayes, Daniel J Gorso, Leslie S Babonis, Mark Q Martindale, Joseph F Ryan Morphological and dietary changes encoded in the genome of Beroe ovata, a ctenophore-eating ctenophore Journal Article In: NAR Genomics and Bioinformatics, vol. 6, iss. 2, 2024. Links | BibTeX | Tags: Beroe ovata, Ctenophora, genome @article{nokey, |
Dorothy Mitchell; Allison Edgar; Júlia Ramon Mateu; Joseph F. Ryan; Mark Q. Martindale The ctenophore Mnemiopsis leidyi deploys a rapid injury response dating back to the last common animal ancestor Journal Article In: Communications Biology, vol. 7, iss. 203, 2024. Links | BibTeX | Tags: Ctenophora, gene regulation, regeneration, whole-body regeneration @article{nokey, |
2023 |
Labib Rouhana; Allison Edgar; Fredrik Hugosson; Valeria Dountcheva; Mark Q. Martindale; Joseph F. Ryan Cytoplasmic polyadenylation is an ancestral hallmark of early development in animals Journal Article In: Molecular Biology and Evolution, vol. 40, iss. 6, 2023. Abstract | Links | BibTeX | Tags: Cnidaria, Ctenophora, cytoplasmic polyadenylation, Evolution, post-transcriptional regulation @article{Rouhana_2023, Differential regulation of gene expression has produced the astonishing diversity of life on Earth. Understanding the origin and evolution of mechanistic innovations for control of gene expression is therefore integral to evolutionary and developmental biology. Cytoplasmic polyadenylation is the biochemical extension of polyadenosine at the 3′-end of cytoplasmic mRNAs. This process regulates the translation of specific maternal transcripts and is mediated by the Cytoplasmic Polyadenylation Element-Binding Protein family (CPEBs). Genes that code for CPEBs are amongst a very few that are present in animals but missing in nonanimal lineages. Whether cytoplasmic polyadenylation is present in non-bilaterian animals (i.e., sponges, ctenophores, placozoans, and cnidarians) remains unknown. We have conducted phylogenetic analyses of CPEBs, and our results show that CPEB1 and CPEB2 subfamilies originated in the animal stem lineage. Our assessment of expression in the sea anemone, Nematostella vectensis (Cnidaria), and the comb jelly, Mnemiopsis leidyi (Ctenophora), demonstrates that maternal expression of CPEB1 and the catalytic subunit of the cytoplasmic polyadenylation machinery (GLD2) is an ancient feature that is conserved across animals. Furthermore, our measurements of poly(A)-tail elongation reveal that key targets of cytoplasmic polyadenylation are shared between vertebrates, cnidarians, and ctenophores, indicating that this mechanism orchestrates a regulatory network that is conserved throughout animal evolution. We postulate that cytoplasmic polyadenylation through CPEBs was a fundamental innovation that contributed to animal evolution from unicellular life. |
2022 |
Allison Edgar; José Miguel Ponciano; Mark Q. Martindale Ctenophores are direct developers that reproduce continuously beginning very early after hatching Journal Article In: Proceedings of the National Academy of Sciences, vol. 119, no. 18, 2022. Abstract | Links | BibTeX | Tags: Ctenophora, dissogeny, Evolution, larval reproduction, life history, Mnemiopsis leidyi @article{Edgar_2022, A substantial body of literature reports that ctenophores exhibit an apparently unique life history characterized by biphasic sexual reproduction, the first phase of which is called larval reproduction or dissogeny. Whether this strategy is plastically deployed or a typical part of these species’ life history was unknown. In contrast to previous reports, we show that the ctenophore Mnemiopsis leidyi does not have separate phases of early and adult reproduction, regardless of the morphological transition to what has been considered the adult form. Rather, these ctenophores begin to reproduce at a small body size and spawn continuously from this point onward under adequate environmental conditions. They do not display a gap in productivity for metamorphosis or other physiological transition at a certain body size. Furthermore, nutritional and environmental constraints on fecundity are similar in both small and large animals. Our results provide critical parameters for understanding resource partitioning between growth and reproduction in this taxon, with implications for management of this species in its invaded range. Finally, we report an observation of similarly small-size spawning in a beroid ctenophore, which is morphologically, ecologically, and phylogenetically distinct from other ctenophores reported to spawn at small sizes. We conclude that spawning at small body size should be considered as the default, on-time developmental trajectory rather than as precocious, stress-induced, or otherwise unusual for ctenophores. The ancestral ctenophore was likely a direct developer, consistent with the hypothesis that multiphasic life cycles were introduced after the divergence of the ctenophore lineage. |
Julia Ramon-Mateu; Allison Edgar; Dorothy Mitchell; Mark Q. Martindale Studying Ctenophora WBR Using Mnemiopsis leidyi Book Section In: Simon Blanchoud; Brigitte Galliot (Ed.): Methods in Molecular Biology, vol. 2450, pp. 95–119, Springer US, 2022. Abstract | Links | BibTeX | Tags: Ctenophora, Husbandry, live imaging, Mnemiopsis leidyi, surgeries, time-lapse, whole-body regeneration, wound healing @incollection{Ramon_Mateu_2022, Ctenophores, also known as comb jellies, are a clade of fragile holopelagic, carnivorous marine inverte- brates, that represent one of the most ancient extant groups of multicellular animals. Ctenophores show a remarkable ability to regenerate in the adult form, being capable of replacing all body parts (i.e., whole- body regeneration) after loss/amputation. With many favorable experimental features (optical clarity, stereotyped cell lineage, multiple cell types), a full genome sequence available and their early branching phylogenetic position, ctenophores are well placed to provide information about the evolution of regener- ative ability throughout the Metazoa. Here, we provide a collection of detailed protocols for use of the lobate ctenophore Mnemiopsis leidyi to study whole-body regeneration, including specimen collection, husbandry, surgical manipulation, and imaging techniques. |
2021 |
Dorothy G. Mitchell; Allison Edgar; Mark Q. Martindale Improved histological fixation of gelatinous marine invertebrates Journal Article In: Frontiers in Zoology, vol. 18, no. 29, 2021. Abstract | Links | BibTeX | Tags: Ctenophora, fixation, immunohistochemistry, in situ hybridization, Mnemiopsis leidyi, Preservation of zooplankton @article{Mitchell_2021, Background Gelatinous zooplankton can be difficult to preserve morphologically due to unique physical properties of their cellular and acellular components. The relatively large volume of mesoglea leads to distortion of the delicate morphology and poor sample integrity in specimens prepared with standard aldehyde or alcohol fixation techniques. Similar challenges have made it difficult to extend standard laboratory methods such as in situ hybridization to larger juvenile ctenophores, hampering studies of late development. Results We have found that a household water repellant glass treatment product commonly used in laboratories, Rain-X®, alone or in combination with standard aldehyde fixatives, greatly improves morphological preservation of such delicate samples. We present detailed methods for preservation of ctenophores of diverse sizes compatible with long-term storage or detection and localization of target molecules such as with immunohistochemistry and in situ hybridization and show that this fixation might be broadly useful for preservation of other delicate marine specimens. Conclusion This new method will enable superior preservation of morphology in gelatinous specimens for a variety of downstream goal. Extending this method may improve the morphological fidelity and durability of museum and laboratory specimens for other delicate sample types. |
Allison Edgar; Dorothy G. Mitchell; Mark Q. Martindale Whole-Body Regeneration in the Lobate Ctenophore Mnemiopsis leidyi Journal Article In: Genes, vol. 12, iss. 6, pp. 867, 2021. Abstract | Links | BibTeX | Tags: Ctenophora, Mnemiopsis leidyi, regeneration @article{Edgar_2021, Ctenophores (a.k.a. comb jellies) are one of the earliest branching extant metazoan phyla. Adult regenerative ability varies greatly within the group, with platyctenes undergoing both sexual and asexual reproduction by fission while others in the genus Beroe having completely lost the ability to replace missing body parts. We focus on the unique regenerative aspects of the lobate ctenophore, Mnemiopsis leidyi, which has become a popular model for its rapid wound healing and tissue replacement, optical clarity, and sequenced genome. M. leidyi’s highly mosaic, stereotyped development has been leveraged to reveal the polar coordinate system that directs whole-body regeneration as well as lineage restriction of replacement cells in various regenerating organs. Several cell signaling pathways known to function in regeneration in other animals are absent from the ctenophore’s genome. Further research will either reveal ancient principles of the regenerative process common to all animals or reveal novel solutions to the stability of cell fates and whole-body regeneration. |
Publications
2024 |
Morphological and dietary changes encoded in the genome of Beroe ovata, a ctenophore-eating ctenophore Journal Article In: NAR Genomics and Bioinformatics, vol. 6, iss. 2, 2024. |
The ctenophore Mnemiopsis leidyi deploys a rapid injury response dating back to the last common animal ancestor Journal Article In: Communications Biology, vol. 7, iss. 203, 2024. |
2023 |
Cytoplasmic polyadenylation is an ancestral hallmark of early development in animals Journal Article In: Molecular Biology and Evolution, vol. 40, iss. 6, 2023. |
2022 |
Ctenophores are direct developers that reproduce continuously beginning very early after hatching Journal Article In: Proceedings of the National Academy of Sciences, vol. 119, no. 18, 2022. |
Studying Ctenophora WBR Using Mnemiopsis leidyi Book Section In: Simon Blanchoud; Brigitte Galliot (Ed.): Methods in Molecular Biology, vol. 2450, pp. 95–119, Springer US, 2022. |
2021 |
Improved histological fixation of gelatinous marine invertebrates Journal Article In: Frontiers in Zoology, vol. 18, no. 29, 2021. |
Whole-Body Regeneration in the Lobate Ctenophore Mnemiopsis leidyi Journal Article In: Genes, vol. 12, iss. 6, pp. 867, 2021. |