Active torque generation for spiralian chiral cleavage
Biophysics
Evolutionary Cell and Developmental Biology (Zoology)
Final Report Abstract
The diversity of animal forms—generated by evolution—is stunning. The animal forms we see around us are generated primarily through developmental processes. Interestingly, the diversity of animal development is remarkably different from that of the adult form. Similar looking animals may arise through very divergent developmental paths and conversely, widely different adult forms may be generated through seemingly highly conserved early development processes. In this work, we have focused on a relatively rarely studied mode of early embryonic development, the so-called spiral cleavage, that is characteristic for a very diverse group of animals named Spiralians, which are spread across the tree of life. We investigated the cellular and biophysical mechanisms that lead to the stereotypic cell division pattern of Spiralian embryos using a prototypical example of this developmental mode, the marine annelid Platynereis dumerillii. Building on the deep understanding of symmetry breaking mechanism operating in the previously studied embryos of nematodes that exhibits a different morphological mode of early development, we asked to what degree similar cell biological mechanisms are at play in the two systems and if so how are they deployed to give rise to the significantly different morphological outcomes. Using high-end microscopy techniques and universal transient labeling procedures, we were able to collect a lot of new data about the dynamic behavior of key cytoskeletal components of the cell during the spiral cleavage. We complemented this data with molecular dissection of gene regulation occurring during this important developmental period. Finally, we used the unique capabilities of our interdisciplinary team to apply quantitative image analysis and physical modeling to the imaging data in order to test the previously established models of symmetry breaking in the new context. Since most of the work was performed on a species that wasn’t previously used for this type of cell biophysical investigation, we had to optimize many existing techniques and develop new ones. Some approaches, especially the ones involving selective reduction of activities of specific genes and pathways, proved impractical in the marine annelid model. Nevertheless, we were able to establish that cortical actin flows play a major role in establishing the slight inclination in the orientation of one specific cell division during spiral cleavage. This seemingly small change in dynamics of intracellular movements results in the specific morphological signature that is shared by one third of the species across the tree of life. Interestingly, it is the very same mechanism that breaks the symmetry in the morphologically distinct annelid embryos. This points to the conclusion that small modifications of universally conserved cellular mechanisms can have large consequences for morphological evolution. Understanding how the underlying cellular processes are regulated in the different developmental contexts remains an exciting challenge for future research.
