Abstract
Shaping the primordia during development relies on forces and mechanisms able to control cell segregation. In the imaginal discs of Drosophila the cellular populations that will give rise to the dorsal and ventral parts on the wing blade are segregated and do not intermingle. A cellular population that becomes specified by the boundary of the dorsal and ventral cellular domains, the so-called organizer, controls this process. In this paper we study the dynamics and stability of the dorsal-ventral organizer of the wing imaginal disc of Drosophila as cell proliferation advances. Our approach is based on a vertex model to perform in silico experiments that are fully dynamical and take into account the available experimental data such as: cell packing properties, orientation of the cellular divisions, response upon membrane ablation, and robustness to mechanical perturbations induced by fast growing clones. Our results shed light on the complex interplay between the cytoskeleton mechanics, the cell cycle, the cell growth, and the cellular interactions in order to shape the dorsal-ventral organizer as a robust source of positional information and a lineage controller. Specifically, we elucidate the necessary and sufficient ingredients that enforce its functionality: distinctive mechanical properties, including increased tension, longer cell cycle duration, and a cleavage criterion that satisfies the Hertwig rule. Our results provide novel insights into the developmental mechanisms that drive the dynamics of the DV organizer and set a definition of the so-called Notch fence model in quantitative terms.
Highlights
Patterning processes in multicellular organisms rely on faithful mechanisms of cell segregation and segmentation [1,2]
How does the DV organizer robustly deal with the cellular growth in order to prevent cell mixing? how can the organizer be conveniently scaled as the tissue grows? we address these questions using a computational approach that takes into account the available experimental data
We propose an in silico framework that sheds light into the dynamics that shape the DV organizer for being an effective source of positional information and a cellular lineage controller
Summary
Patterning processes in multicellular organisms rely on faithful mechanisms of cell segregation and segmentation [1,2]. The concept of compartment implies the existence of non-trivial boundaries that control cell migration [16,17,18,19] While these lineage frontiers are not necessarily associated with morphological hallmarks of the organism, they play in all cases an additional and all-important role for setting the developmental plan. An organizer acts in practice as the coordinate axis of a reference system To this end an organizer must display some key features to guarantee its reliability as a source of positional information: the width of this cell population is constricted to few (two, three) cells [26,27] and they develop maintaining a straight shape [28,29]. These findings meant a major breakthrough in modern Developmental Biology because of its powerful conceptual implications in terms of the modular design of multicellular organisms, conserved in both vertebrates and invertebrates, and its genetic foundation
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