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Modepalli, V.

Publications and source records attributed to Modepalli, V..

7 recordsLinked to original sources

De-novo Genome of the Edwardsiid anthozoan Edwardsia elegans

Cnidarians (sea anemones, corals, hydroids, and jellyfish) are a key outgroup for comparisons with bilaterial animals to trace the evolution of genomic complexity and diversity within the animal kingdom, as they separated from most other animals 100s of millions of years ago. Cnidarians have extensive diversity, yet the paucity of genomic resources limits our ability to compare genomic variation between cnidarian clades and species. Here we report the genome for Edwardsia elegans, a sea anemone in the most specious genus of the family Edwardsiidae, a phylogenetically important family of sea anemones that contains the model anemone Nematostella vectensis. The E. elegans genome is 396 Mb and predicted to encode approximately 49,000 proteins. We annotated large conservation of macrosynteny between E. elegans and other Edwardsiidae anemones as well as conservation of both microRNAs and ultra conserved noncoding elements previously reported in other cnidarians species. We also highlight microsyntenic variation of clustered developmental genes and ancient gene clusters that vary between species of sea anemones, despite previous research showing conservation between cnidarians and bilaterians. Overall, our analysis of the E. elegans genome highlights the importance of using multiple species to represent a taxonomic group for genomic comparisons, where genomic variation can be missed for large and diverse clades.

genomics↗

Plant-like heliotropism in a photosymbiotic animal

Being photosynthetic sessile organisms, plants established heliotropism to track the suns position across the sky and allow their vegetative parts to orient accordingly. Here, we report plant-like heliotropic movement in a photosymbiotic sea anemone Anemonia viridis. Like plants, photosynthesis represents a key energy source in endosymbiotic cnidarians bearing microalgae. We observed that A. viridis in their natural habitats under sunlight displayed heliotropism or solar tracking by pointing their tentacles towards the sun while remaining sessile, facing east at dawn and west at dusk as they track the suns relative position through the day, a phenomenon previously only observed in plants. Solar tracking movements in A. viridis are driven by a light wavelength that prompts photosynthesis in their endosymbionts. The heliotropic response was absent in both bleached (aposymbiotic) A. viridis and in symbiotic A. viridis with chemically inhibited photosynthesis. We revealed a direct correlation between heliotropism and endosymbiont oxygen production in A. viridis. Our findings suggest that photosymbiotic A. viridis has likely evolved plant-like heliotropism as an effective way to modulate exposure to solar irradiation for photosynthesis. The study exemplifies how photosynthetic organisms such as plants and photosymbiotic sea anemones, display similar behaviour in response to similar environmental pressures.

animal behavior and cognition↗

Gene regulatory network that shaped the evolution of larval sensory organ in Cnidaria

Among non-bilaterian animals, a larval apical sensory organ with integrated neurons is only found in cnidarians. Within cnidarians, an apical organ with a ciliary tuft is mainly found in Actiniaria. Whether this apical tuft has evolved independently in Actiniaria or alternatively originated in the common ancestor of Cnidaria and Bilateria and was lost in specific groups is uncertain. We generated transcriptomes of the apical domain during the planula stage of four species representing three key groups of cnidarians: Aurelia aurita (Scyphozoa), Nematostella vectensis (Actiniaria), and Acropora millepora & Acropora tenuis (Scleractinia). We showed that the canonical genes implicated in patterning the apical domain of Nematostella are largely absent in Aurelia, indicating that scyphozoans and anthozoans do not share apical organ homology. In contrast, the apical domain of the scleractinian planula shares gene expression pattern with Nematostella. By comparing the larval single-cell transcriptomes, we revealed the apical organ cell type of Scleractinia and confirmed its homology to Actiniaria. However, Fgfa2, a vital regulator of the regionalisation of the Nematostella apical organ, is absent in the scleractinian genome. Likewise, we found that FoxJ1 and 245 genes associated with cilia are exclusively expressed in the Nematostella apical domain, which is in line with the presence of ciliary apical tuft in Actiniaria and its absence in Scleractinia and Scyphozoa. Our findings suggest that the common ancestor of cnidarians and bilaterians lacked an apical organ with a ciliary tuft, and it could have evolved independently in several clades of cnidarians and bilaterians.

evolutionary biology↗

Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensis

The apical pole of eumetazoan ciliated larvae acts as a neurosensory structure and is principally composed of sensory-secretory cells. Cnidarians like the sea anemone Nematostella vectensis are the only non-bilaterian group to evolve ciliated larvae with a neural integrated sensory organ that is likely homologous to bilaterians. Here, we uncovered the molecular signature of the larval sensory organ in Nematostella by generating a transcriptome of the apical tissue. We characterised the cellular identity of the apical domain by integrating larval single-cell data with the apical transcriptome and further validated this through in-situ hybridisation. We discovered that the apical domain comprises a minimum of 6 distinct cell types, including apical cells, neurons, peripheral flask-shaped gland/secretory cells, and undifferentiated cells. By profiling the spatial expression of neuronal genes, we showed that the apical region has a unique neuronal signature distinct from the rest of the body. By combining the planula cilia proteome with the apical transcriptome data, we revealed the sheer complexity of the non-motile apical tuft. Overall, we present comprehensive spatial/molecular data on the Nematostella larval sensory organ and open new directions for elucidating the functional role of the apical organ and larval nervous system.

evolutionary biology↗

Regeneration in sponge Sycon ciliatum mimics postlarval development

Somatic cells dissociated from an adult sponge can re-organize and develop into a functional juvenile. However, the extent to which regeneration recapitulates embryonic developmental signaling pathways has remained enigmatic for more than a century. To this end, we have standardized and established a sponge Sycon ciliatum regeneration protocol to achieve consistent regeneration in cell culture. From the morphological analysis, we demonstrated that dissociated sponge cells follow a series of morphological events resembling embryonic and postlarval development. Hence, we propose that sponge regeneration represents somatic development. To support our hypothesis, we performed high-throughput sequencing on regenerating samples and compared the data with regular embryonic and postlarval development of Sycon ciliatum. Our comparative transcriptomic analysis illuminates that sponge regeneration is equally as dynamic as embryogenesis. We find that sponge regeneration is orchestrated by complex regulatory mechanisms by recruiting signaling pathways like those utilized in embryonic development to organize into a functional juvenile. In the current study, we lay down the basic framework to study Sycon ciliatum regeneration. Since sponges are likely to be the first branch of extant multicellular animal and the sister lineage to nearly all animals, we suggest that this system can be explored to study the genetic features underlying the evolution of multicellularity and regeneration.

developmental biology↗

Unravelling the developmental and functional significance of an ancient Argonaute duplication

microRNAs (miRNAs), base-pair to messenger RNA targets and guide Argonaute proteins to mediate their silencing. This target regulation is considered crucial for animal physiology and development. However, this notion is based exclusively on studies in bilaterians, which comprise almost all lab model animals. To fill this glaring phylogenetic gap, we characterized the functions of two Argonaute paralogs in the sea anemone Nematostella vectensis of the phylum Cnidaria, which is separated from bilaterians by [~]600 million years. Using genetic manipulation, Argonaute-immunoprecipitations and high-throughput sequencing we provide experimental evidence for the developmental importance of miRNAs in a non-bilaterian animal. Additionally, we uncover unexpected differential distribution of distinct miRNAs between the two Argonautes and the ability of one of them to load additional types of small RNAs. This enables us to postulate a novel model for evolution of miRNA precursors in sea anemones and their relatives, revealing alternative trajectories for metazoan miRNA evolution.

evolutionary biology↗

Dynamics of venom composition across a complex life cycle

Little is known about venom in young developmental stages of animals. The appearance of stinging cells in very early life stages of the sea anemone Nematostella vectensis suggests that toxins and venom are synthesized already in eggs, embryos and larvae of this species. Here we harness transcriptomic and biochemical tools as well as transgenesis to study venom production dynamics in Nematostella. We find that the venom composition and arsenal of toxin-producing cells change dramatically between developmental stages of this species. These findings might be explained by the vastly different ecology of the larva and adult polyp as sea anemones develop from a miniature non-feeding mobile planula to a much larger sessile polyp that predates on other animals. Further, the results suggest a much wider and dynamic venom landscape than initially appreciated in animals with a complex life cycle.

evolutionary biology↗