Multi-tissue analysis of embryonic axis elongation using transgenic quails and time-lapse imaging – MULTIEL

Posterior axis elongation is a major morphogenetic event that produces the typical head-to-tail elongated body shape of vertebrate embryos. Axis elongation involves the three germ layers of the embryo: the ectoderm, the mesoderm, and the endoderm. Interactions between these layers represent a fundamental aspect of developmental biology; they allow for the patterning and morphogenesis of the different functioning organs. However, while the mechanisms of tissue elongation have mostly been studied in separate tissue types, the principles allowing for the coordination of elongation between tissues and between germ layers remain largely unknown. Additionally, the mechanisms defining the coordination between cellular fate decisions, cellular movements, and axis elongation remain to be discovered.
MULTIEL will build on our previous work where we used transgenic quail embryos that ubiquitously express a nuclear fluorescent protein and time-lapse imaging to quantitatively compare different tissue movements in the elongating embryo. This approach allowed us to demonstrate that embryonic elongation is defined by the coordination of distinct tissue-specific behaviors. In particular, we observed that the posterior tissue layers extend differentially, sliding in independent directions and speeds relative to one another. Of importance for this project, our data indicate that the regulation of cells leaving the embryonic tail bud, an area that contains progenitor cells, is central to coordinate this multi-tissue elongation choreography. However, neither the single cell behaviors nor the exact contributions of progenitor cells to the different embryonic tissues have ever been assessed. Interestingly, the progenitor region is precisely the place where cell specification related to tissue formation takes place: progenitors adopt either a mesoderm or a neuro-ectoderm fate before migrating into their future tissues. In the preliminary data, we show that differential expression of tissue-specific proteins (Sox2 for neural tissue and Bra for mesodermal tissue) divides the progenitor region into sub-domains. These data suggest that these sub-domains, because they contain cells expressing different levels of Sox2 and Bra, might contribute in unique ways to axis formation.
In MULTIEL, we hypothesize that specification events taking place in the progenitor region interplay with morphogenesis to build the different tissues of the body axis. We propose to address the coordination of cell fate specification and morphogenesis by using live imaging microscopy and newly generated transgenic quail embryos that allow for both single cell and tissue movement analysis with an exceptional level of precision. Specific objectives of MULTIEL are: 1) deciphering cell and tissue behaviors in the progenitor zone and its derivative tissues and 2) analyzing the coordination of cell specification and morphogenesis during axis elongation. The outcome of this project will contribute to our basic knowledge of vertebrate embryo axis elongation and on the coordination of morphogenesis and cell fate acquisition during development.