Spatiotemporal development of coexisting wave domains of Rho activity in the cell cortex

The Rho family GTPases are molecular switches that regulate cytoskeletal dynamics and cell movement through a complex spatiotemporal organization of their activity. In Patiria miniata (starfish) oocytes under in vitro experimental conditions (with overexpressed Ect2, induced expression of Δ90 cyclin B, and roscovitine treatment), such activity generates multiple co-existing regions of coherent propagation of actin waves. Here we use computational modeling to investigate the development and properties of such wave domains. The model reveals that the formation of wave domains requires a balance between the activation and inhibition in the Rho signaling motif. Intriguingly, the development of the wave domains is preceded by a stage of low-activity quasi-static patterns, which may not be readily observed in experiments. Spatiotemporal patterns of this stage and the different paths of their destabilization define the behavior of the system in the later high-activity (observable) stage. Accounting for a strong intrinsic noise allowed us to achieve good quantitative agreement between simulated dynamics in different parameter regimes of the model and different wave dynamics in Patiria miniata and wild type Xenopus laevis (frog) data. For quantitative comparison of simulated and experimental results, we developed an automated method of wave domain detection, which revealed a sharp reversal in the process of pattern formation in starfish oocytes. Overall, our findings provide an insight into spatiotemporal regulation of complex and diverse but still computationally reproducible cell-level actin dynamics.

Polarized Dishevelled dissolution and condensation drives embryonic axis specification in oocytes

The organismal body axes that are formed during embryogenesis are intimately linked to intrinsic asymmetries established at the cellular scale in oocytes. Here, we report an axis-defining event in meiotic oocytes of the sea star Patiria miniata. Dishevelled is a cytoplasmic Wnt pathway effector required for axis development in diverse species, but the mechanisms governing its function and distribution remain poorly defined. Using time-lapse imaging, we find that Dishevelled localizes uniformly to puncta throughout the cell cortex in Prophase I-arrested oocytes, but becomes enriched at the vegetal pole following meiotic resumption through a dissolution-condensation mechanism. This process is driven by an initial disassembly phase of Dvl puncta, followed by selective reformation of Dvl assemblies at the vegetal pole. Rather than being driven by Wnt signaling, this localization behavior is coupled to meiotic cell cycle progression and influenced by Lamp1+ endosome association and Frizzled receptors pre-localized within the oocyte cortex. Our results reveal a cell cycle-linked mechanism by which maternal cellular polarity is transduced to the embryo through spatially-regulated Dishevelled dynamics.

Spatiotemporal development of coexisting wave domains of Rho activity in the cell cortex

The Rho family GTPases are molecular switches that regulate cytoskeletal dynamics and cell movement through a complex spatiotemporal organization of their activity. In Patiria miniata (starfish) oocytes, such activity generates multiple co-existing regions of coherent propagation of actin waves. Here we use computational modeling to investigate the development and properties of such wave domains. The model reveals that the formation of wave domains requires a balance of the autocatalytic activation and the negative feedback in the Rho signaling motif. Intriguingly, the development of the wave domains is preceded by a stage of low-activity quasi-static patterns, which may not be readily observed in experiments. Spatiotemporal patterns of this stage and the different paths of their destabilization define the behavior of the system in the later high-activity (observable) stage. Accounting for a strong intrinsic noise allowed us to reproduce wave dynamics in both Patiria miniata and Xenopus laevis (frog). For quantitative comparison of simulated and experimental results, we developed an automated method of wave domain detection, which revealed a sharp reversal of pattern formation in the middle of anaphase in starfish oocytes. Overall, our findings provide an insight into spatiotemporal regulation of complex and diverse but still computationally reproducible cell-level actin dynamics.

Developmental transcriptomes of the sea star, Patiria miniata, illuminate how gene expression changes with evolutionary distance

Understanding how changes in developmental gene expression alter morphogenesis is a fundamental problem in development and evolution. A promising approach to address this problem is to compare the developmental transcriptomes between related species. The echinoderm phylum consists of several model species that have significantly contributed to the understanding of gene regulation and evolution. Particularly, the regulatory networks of the sea star, Patiria miniata (P. miniata), have been extensively studied, however developmental transcriptomes for this species were lacking. Here we generated developmental transcriptomes of P. miniata and compared these with those of two sea urchins species. We demonstrate that the conservation of gene expression depends on gene function, cell type and evolutionary distance. With increasing evolutionary distance the interspecies correlations in gene expression decreases. The reduction is more severe in the correlations between morphologically equivalent stages (diagonal elements) than in the correlation between morphologically distinct stages (off-diagonal elements). This could reflect a decrease in the morphological constraints compared to other constraints that shape gene expression at large evolutionary divergence. Within this trend, the interspecies correlations of developmental control genes maintain their diagonality at large evolutionary distance, and peak at the onset of gastrulation, supporting the hourglass model of phylotypic stage conservation.

Developmental transcriptomes of the sea star, Patiria miniata, illuminate the relationship between conservation of gene expression and morphological conservation

Evolutionary changes in developmental gene expression lead to alteration in the embryonic body plan and biodiversity. A promising approach for linking changes in developmental gene expression to altered morphogenesis is the comparison of developmental transcriptomes of closely related and further diverged species within the same phylum. Here we generated quantitative transcriptomes of the sea star, Patiria miniata (P. miniata) of the echinoderm phylum, at eight embryonic stages. We then compared developmental gene expression between P. miniata and the sea urchin, Paracentrotus lividus (~500 million year divergence) and between Paracentrotus lividus and the sea urchin, Strongylocentrotus purpuratus (~40 million year divergence). We discovered that the interspecies correlations of gene expression level between morphologically equivalent stages decreases with increasing evolutionary distance, and becomes more similar to the correlations between morphologically distinct stages. This trend is observed for different sub-sets of genes, from various functional classes and embryonic territories, but is least severe for developmental genes sub-sets. The interspecies correlation matrices of developmental genes show a consistent peak at the onset of gastrulation, supporting the hourglass model of phylotypic stage conservation. We propose that at large evolutionary distance the conservation of relative expression levels for most sets of genes is more related to the required quantities of transcripts in a cell than to conserved morphogenesis processes. In these distances, the information about morphological similarity is reflected mostly in the interspecies correlations between the expressions of developmental control genes.Author summaryUnderstanding the relationship between the interspecies conservation of gene expression and morphological similarity is a major challenge in modern evolutionary and developmental biology. The Interspecies correlations of gene expression levels have been used extensively to illuminate these relationships and reveal the developmental stages that show the highest conservation of gene expression, focusing on the diagonal elements of the correlation matrices. Here we generated the developmental transcriptomes of the sea star, Patiria miniata, and used them to study the interspecies correlations between closely related and further diverged species within the echinoderm phylum. Our study reveals that the diagonal elements of the correlation matrices contain only partial information. The off-diagonal elements, that compare gene expression between distinct developmental stages, indicate whether the conservation of gene expression is indeed related to similar morphology or instead, to general cellular constraints that linger throughout development. With increasing evolutionary distances the diagonal elements decrease and become similar to the off-diagonal elements, reflecting the shift from morphological to general cellular constraints. Within this trend, the interspecies correlations of developmental control genes maintain their diagonality even at large evolutionary distance, and peak at the onset of gastrulation, supporting the hourglass model of phylotypic stage conservation.

GENOMA: a multilevel platform for marine biology

Next-generation sequencing (NGS) technologies are greatly facilitating the sequencing of whole genomes leading to the production of different gene annotations, released often from both reference resources (such as NCBI or Ensembl) and specific consortia. All these annotations are in general very heterogeneous and not cross-linked, providing ambiguous knowledge to the users. In order to give a quick view of what is available, and trying to centralize all the genomic information of reference marine species, we set up GENOMA (GENOmes for MArine biology). GENOMA is a multilevel platform that includes all the available genome assemblies and gene annotations about 12 species (Acanthaster planci, Branchiostoma floridae, Ciona robusta, Ciona savignyi, Gasterosteus aculeatus, Octopus bimaculoides, Patiria miniata, Phaeodactylum tricornutum, Ptychodera flava and Saccoglossus kowalevskii). Each species has a dedicated JBroswe and web page, where is summarized the comparison between the different genome versions and gene annotations available, together with the possibility to directly download all the information. Moreover, an interactive table including the union of different gene annotations is also consultable on-line. Finally, a query page system that allows to search specific features in one or more annotations simultaneously, is embedded in the platform. GENOMA is publicly available at http://bioinfo.szn.it/genoma/.

GENOMA: a multilevel platform for marine biology

Next-generation sequencing (NGS) technologies are greatly facilitating the sequencing of whole genomes leading to the production of different gene annotations, released often from both reference resources (such as NCBI or Ensembl) and specific consortia. All these annotations are in general very heterogeneous and not cross-linked, providing ambiguous knowledge to the users. In order to give a quick view of what is available, and trying to centralize all the genomic information of reference marine species, we set up GENOMA (GENOmes for MArine biology). GENOMA is a multilevel platform that includes all the available genome assemblies and gene annotations about 12 species (Acanthaster planci, Branchiostoma floridae, Ciona robusta, Ciona savignyi, Gasterosteus aculeatus, Octopus bimaculoides, Patiria miniata, Phaeodactylum tricornutum, Ptychodera flava and Saccoglossus kowalevskii). Each species has a dedicated JBroswe and web page, where is summarized the comparison between the different genome versions and gene annotations available, together with the possibility to directly download all the information. Moreover, an interactive table including the union of different gene annotations is also consultable on-line. Finally, a query page system that allows to search specific features in one or more annotations simultaneously, is embedded in the platform. GENOMA is publicly available at http://bioinfo.szn.it/genoma/.