To understand the deep origins of animal diversity, we compare mechanisms of development and cell-cell adhesion mainly using Drosophila and the spider Parasteatoda tepidariorum.
Multicellular animals, the Metazoa, show a great diversity of body forms. Fossil records suggest that the major morphology-based taxonomic groups of metazoans, including the arthropods and chordates, had already existed more than 500 million years ago. Comparative studies of genetic mechanisms underlying the development of body forms in the model vertebrates and invertebrates, such as Xenopus and Drosophila, have revealed some conserved aspects of the developmental mechanisms among the metazoans. However, our understanding of the deeply ancient animals from which the body-form diversity was evolved is still in its infancy. For example, there is no consensus of idea about whether the segmented body plans in the major metazoan groups have common or independent origins. One of the biggest obstacles to reconstructing the macroevolutionary processes is the fact that during evolution the animals flexibly and sometimes drastically changed their genetic programs without disrupting the basic body plan in each major metazoan branch. Our research in BRH aims to overcome this problem and achieve a good understanding of the ancestral animals that were allowed to evolve the great diversity of animal forms. To this end, we compare mechanisms of development and cell-cell adhesion mainly using Drosophila and the spider Parasteatoda tepidariorum (see below for more details).
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Senior ResearcherHiroki ODA,Ph.D.
Post-Doctoral fellowSawa IWASAKI,Ph.D.
Technical assistantAkiko NODA
Our Collaborator Maarten Hilbran,Ph.D. who is from Oxford Brookes University
stayed our laboratory for 2 weeks.
1) Evolution of classical cadherins responsible for adherens junctions
We investigate the diversification of the structure and function of cell-cell adhesion molecules called classical cadherins, which are the key components of the adherens junctions. This junction type is of particular importance in driving and regulating tissue morphogenesis. We have identified lineage-specific structural reductions in the extracellular regions of classical cadherins. Our data suggest that similar but independent structural changes occurred in the classical cadherins at the adherens junctions in several different animal lineages. We are now attempting to investigate the functional significance of the classical cadherin structural changes using Drosophila. We want to understand the impact of evolutionary changes in cell-cell adhesion interfaces on metazoan morphogenesis.
Expression of DE-cadherin during Drosophila gastrulation
2) Development of the spider embryo
Second, using the spider Parasteatoda tepidariorum, a common house spider, we try to identify cellular, genetic and molecular mechanisms of arthropod body plan formation that are distinct from those of Drosophila. We have found that Hedgehog signaling plays key roles in anterior-posterior axis formation in the spider (Fig. 2). In Drosophila, similar roles are played by the Drosophila Bicoid-Nanos system, which is operational only in the syncytial environment. We also showed that cellularization in the spider is complete at or before the 16-nucleus stage, sharply contrasting with the situation of the Drosophila embryo, which is a syncytium until the number of nuclei increases to 6,000. Our findings have revealed that the common arthropod body plan is achieved by largely distinct mechanisms, suggesting that genetic programs underlying the formation of the basic body plan significantly changed during evolution. One of the most important messages from our spider studies is that the diversity of the genetic programs is large even within each major metazoan subbranch (such as the arthropod phylum). Comparative studies of widely-ranged animal species within the subbranch are required to better understand the ancestral states of the arthropod body plan and other bilaterally symmetrical metazoan body plans.
An adult female of the spider Parasteatoda tepidariorum (left) and a developing embryo (right)
1) A "domain-loss" model for classical cadherin evolution
We proposed a “domain-loss” model to explain the diversification of the extracellular structures of classical cadherins that are responsible for adherens junction assembly in the metazoans.
Fig. 1. A “domain-loss” model to explain the diversification of classical cadherin structure.
2) A shortened cadherin can function in adhesion, but not in epithelial bending
We constructed a Drosophila DE-cadherin lacking a half of its extracellular region and found that it can function as an adhesion molecule to organize the blastoderm epithelium but not as a morphogenetic regulator to drive ventral furrow formation, an epithelial bending accompanied by cooperative apical constrictions of cells.
Fig.2. Replacement of DE-cadherin with a shortened one caused specific defects in ventral furrow formation.
3) Hedgehog signaling in global pattering of the sider embryo
We discovered key roles of Hedgehog signaling in anterior-posterior axis formation in the early embryo of the spider Parasteatoda tepidariorum. We also showed that migration of the source of Dpp signal that orients the dorsal-ventral axis depends on the roles of Hedgehog signaling. This work highlighted the crucial importance of Hedgehog signaling in global patterning of the spider embryo.
Fig. 3. Embryonic RNA interference for Hedgehog signaling pathway components results in severe defects in early embryonic patterning.
4) Microinjection is now available for early spider embryos
We succeeded in applying a microinjection technique to early spider embryos. Using this technique, we can perform, for example, cell labeling, exogenous expression of fluorescent protein and embryonic RNA interference. Actually, we used this technique to verify that cellularization is complete at or before the 16-nucleus stage in the spider embryo.
Fig. 4. Cell clone labeling by microinjection of FITC-dextran into single blastomeres in early spider embryos.
5) Stripe-splitting, a novel mode of animal segmentation
We discovered a novel mode of segmentation, stripe-splitting, in the developing head of the spider Parasteatoda tepidariorum embryo. A stripe of hedgehog expression, after traveling, undergoes repeated splitting to pattern the three segmental units in the spider head. Our data suggest that this segmentation strategy employs an autoregulatory signaling network that hedgehog signaling pathway components, orthodenticle and odd-pared participate in. Our findings provide new insights into the evolution of segmented body plans in the metazoans.
Fig. 5. A stripe of hedgehog expression (purple) in the head region (see upper than the brown region) undergoes repeated splitting.
Shigetaka Nishiguchi, Akira Yagi, Nobuaki Sakai, Hiroki Oda（2016）
Divergence of structural strategies for homophilic E-cadherin binding among bilaterians
Journal of Cell Science DOI: 10.1242/jcs.189258
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