Juniorprofessor Steffen LemkeMorphogenesis and the Evolution of Form
Our team takes a fresh look at a textbook model of how animals form from a naïve epithelial tissue. We study how this developmental program diversified and reorganized as new genes, mechanical constraints, and environmental parameters contributed to innovation in tissue remodeling.
Bugs and beetles, birds and flies, fish, frogs, and us humans: all our bodies have been shaped from one simple tissue. In the very early days of our lives, this tissue has folded up into layers, and these layers then became skin and nerves, muscles and bones, gut and lung.
It is this first tissue folding, called gastrulation, that sets up our diverse body plans; without it, animal life in today’s complexity probably would not exist. In its basic principles, this core program of development is used in all animals. In variations, tissue folding determines our appearance and instructs the formation of our organs, both in vivo and in organoids. How this program has diversified and repeatedly reorganized itself is a fundamental unanswered question in biology. Our major passion is to understand this problem by studying gastrulation in a set of different animal species. We reveal innovations in tissue remodeling, namely how cells interact and change their shape, and characterize their regulation through modifications of the cytoskeleton. Our group builds on expertise in animal evolution, development and cell biology, and integrates complementary perspectives from engineers and physicists.
One of the remarkable properties of animals is that they share the same core elements in their cytoskeleton. F-Actin, Myosin, and Microtubules already exist in fungi, sponges, corals and jellyfish, they regulate shape and mechanical properties of cells since the earliest animals, and they remain functional even if swapped between species. Also conserved are many of the genes that set up the molecular coordinate system and provide the growing animal embryo with information about space and time. What remains as a genetic variable to innovate tissue remodeling is the relay of spatial instructions to the motors that establish and change the cytoskeleton. Known molecular mechanisms for such a relay of information are, for instance, signaling cascades and intracellular trafficking.
In addition to genetically encoded signaling molecules and trafficking hubs, abiotic factors (such as temperature and physical constraints) influence relay and interpretation of spatial information. In the early embryo, the effect of such parameters varies with parental life style, habitat, and climate conditions. To shield tissue remodeling from these influences, biological strategies range from chaperoning proteins to the addition of redundant information and an optimal timing of tissue folding.
We address the following major questions
- What characterizes novelty in tissue remodeling?
- How does this novelty emerge from new mechanics in the interaction of cells and tissues?
- How is new tissue folding tied to an optimization of signaling within and between cells?
- How do environment and climate relate to innovation in tissue remodeling?
We use a zoo of different fly species to address these problems. Flies are easy to keep in the lab and their embryos all follow comparable steps of development. These steps can be readily compared to the fruit fly Drosophila, a powerful model system used in laboratories worldwide to study the molecular and physical regulation of tissue remodeling. Our group works interdisciplinary and uses experimental methods ranging from phylogenetics, genome analyses and cell biology to genetics, quantitative imaging and modelling.
- Caroti, F, González Avalos, E, Noeske, V, González Avalos, P, Kromm, D, Wosch, M, Schütz, L, Hufnagel, L and Lemke, S (2018) Decoupling from yolk sac is required for extraembryonic tissue spreading in the scuttle fly Megaselia abdita. eLife 7, e34616.
- Urbansky, S, González Avalos, P, Wosch, M and Lemke, S (2016) Folded gastrulation and T48 drive the evolution of coordinated mesoderm internalization in flies. eLife 5, e18318.
- Kappe, CP, Schütz, L, Gunther, S, Hufnagel, L, Lemke, S, Leitte, H (2015) Reconstruction and Visualization of Coordinated 3D Cell Migration Based on Optical Flow. IEEE VIS 2015.
- Caroti, F, Urbansky, S, Wosch, M, and Lemke, S (2015) Germ line transformation and in vivo labeling of nuclei in Diptera: report on Megaselia abdita (Phoridae) and Chironomus riparius (Chironomidae). Dev Genes Evol 225:179.
- Heermann, S, Schütz, LC, Lemke, S, Krieglstein, K, Wittbrodt, J. (2015) Eye morphogenesis driven by epithelial flow into the optic cup facilitated by modulation of bone morphogenetic protein. eLife 4, e05216.