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Olson, B. J. S. C.

Publications and source records attributed to Olson, B. J. S. C..

2 recordsLinked to original sources

Transcriptome analysis reveals temporally regulated genetic networks during Drosophila border cell collective migration

BackgroundCollective cell migration underlies many essential processes, including sculpting organs during embryogenesis, wound healing in the adult, and metastasis of cancer cells. At mid-oogenesis, Drosophila border cells undergo collective migration. Border cells round up into a small group, detach from the epithelium, and migrate - at first rapidly through the surrounding tissue, then slower, with the cluster rotating several times before stopping at the oocyte. While specific genes that promote cell signaling, polarization of the cluster, formation of protrusions, and cell-cell adhesion are known to regulate border cell migration, there may be additional genes that promote these distinct dynamic phases of border cell migration. Therefore, we sought to identify genes whose expression patterns changed during border cell migration. ResultsWe performed RNA-sequencing on border cells isolated at pre-, mid-, and late-migration stages. We report that 1,729 transcripts, in nine co-expression gene clusters, are temporally and differentially expressed across the three migration stages. Gene ontology analyses and constructed protein-protein interaction networks identified genes expected to function in collective migration, such as regulators of the cytoskeleton, adhesion, and tissue morphogenesis, but also a notable enrichment of genes involved in immune signaling, ribosome biogenesis, and stress responses. Finally, we validated the in vivo expression and function of a subset of identified genes in border cells. ConclusionsOverall, our results identified differentially and temporally expressed genetic networks that may facilitate the efficient development and migration of border cells. The genes identified here represent a wealth of new candidates to investigate the molecular nature of dynamic collective cell migrations in developing tissues.

developmental biology↗

Gene loss during the transition to multicellularity

Multicellular evolution is a major transition associated with momentous diversification of multiple lineages and increased developmental complexity. The volvocine algae comprise a valuable system for the study of this transition, as they span from unicellular to undifferentiated and differentiated multicellular morphologies despite their genomes being highly similar, suggesting multicellular evolution requires few genetic changes to undergo dramatic shifts in developmental complexity. Here, the evolutionary dynamics of six volvocine genomes were examined, where a gradual loss of genes was observed in parallel to the co-option of a few key genes. Protein complexes in the six species exhibited a high degree of novel interactions, suggesting that gene loss plays a role in evolutionary novelty. This finding was supported by gene network modeling, where gene loss outpaces gene gain in generating novel stable network states. These results suggest developmental complexity may be driven by gene loss, and not just by gene gain. Significance StatementIncreased developmental complexity is thought to evolve mainly through genetic innovation and co-option. Comparison of the genomes of the closely related volvocines revealed that despite large changes in developmental complexity their genomes are exhibiting significant gene loss. Further, a burst of gene loss is shown to occur at the transition to undifferentiated multicellularity by gene inactivation and decay. This likely results in changes to protein-protein interactions within the cell, suggesting evolutionary novelty does not always require gene gain. Using empirical and modelling approaches we demonstrate gene loss can more easily produce protein network novelty than gene gain. We propose that gene loss can be a driver of biological innovation, allowing for reconfiguration of gene networks and differential use of existing functional repertoires.

evolutionary biology↗