The making of an organism involves numerous operations that rely heavily on individual and collective cell behaviors. In particular, the structures produced during development acquire their characteristics following the deployment of series of operations that can be grouped into a small number of entities having the status of developmental processes. It remains very difficult, but crucial, to identify developmental processes. Indeed, it is only when identified and when their architecture is recognized that the logic of development and of its evolution begin to be understood.

Elongation is potentially a developmental process. As the embryo of all bilaterian elongates early along its future anterior-posterior axis, this process is probably fundamental and phylogenetically basal. Importantly the morphogenesis of many structures that appear later in the embryo, then in the body, includes a step of elongation. Sometimes, as in the case of the dorso-ventral extension of the surface ectoderm, the involvement of elongation appears only after a detailed analysis of cell behavior. Elongation therefore is very favorable to study the architecture, the evolution and as a result the design of a developmental process. We compare the elongation of the embryo from three chordates (amphioxus for its phylogenetic basal position, close to the urbilaterian, zebrafish and mouse) and also late structures in these same species (in particular, hair follicles in the mouse). These phylo- and onto-genetic comparisons of elongation should also help discovering the conditions and constraints of the evolution of a developmental process.

The comparison of the elongation of hair follicles and the mouse embryo for which new results were obtained in 2010 deserves mention. The elongation of the hair follicle mobilizes a special pool of cells whose proliferation, that follows a strict stem mode, and oriented divisions organized the hair follicle into proximo-distal clonal columns. Moreover, the contribution of the descendants of several stem cells to each column is obtained by mobilizing a process of cell intercalation. This applies to all concentric layers of the HF except to the outer most layer whose elongation involves an exponential mode of proliferation – not a stem mode – which, combined with cell death, adjust its growth to the linear one of the internal layers. The unexpected complexity of HF elongation contrasts with the elongation process used by the renal tubules or the neuronal columns in the cortical structures of the central nervous system that are based solely on oriented cell divisions combined with (respectively) an exponential or stem mode of growth.

The elongation of the mouse embryo also concerns several tissues and cover a long period (from gastrulation to late tail bud stage). To the previously obtained information on the elongation of myotome and posterior nervous system that involve pools of stem cells located caudally and, again, a process of cell intercalation, we should add the following novel findings: during the elongation of the embryonic axis, we detected cells that contribute to - but only to - mesodermal and neural tissues (the N-M progenitors) and this even during the tail bud stage. These cells have characteristics of stem cells and the N-M progenitor pool may overlap or be clonally very close to those giving rise to respectively the myotome and central nervous system. This challenge the paradigm that the three germ layers, formed by gastrulation, constitute the primary branchpoints in differentiation of the pluripotent epiblast and adds to the complexity of the elongation process of the embryo. It highlights the need to now follow directly, using 4D imaging, cell behaviors in this pool of cells.

Clearly, these comparisons show that the mechanisms of elongation of different structures use combinations of the very same basic operations. Elongation corresponds therefore to a genuine developmental process in that the elongation of the different embryonic and adult structures and of the embryo itself seems to have been elaborated from what corresponds for the development to an entity. Our future phylogenetic and ontogenetic comparisons will further highlight the differences between the various mechanisms of elongation and thus reveal both the constraints and the plasticity of this important developmental process.

In parallel, our study of zebrafish myotome morphogenesis unravelled the mechanism underlying the establishment within the myotome of a central compartment that exhibits an organisational role on the myotome itself as well as surrounding tissues such as motoneurons and lateral line sensory organs. Our results show that extracellular matrix Laminins, via Heparan Sulfate Proteoglycans, are instrumental in patterning Bmp responsiveness in the myotome, excluding it from the central compartment and thereby allowing for its establishment. Our study underlines the importance of extracellular cues for the precise spatial modulation of cell response to morphogens.

Keywords: mouse embryo / clonal analysis / 4D imaging / central nervous system / muscular system / hair follicle / amphioxus / zebrafish / developmental biology / LaacZ / chordates / elongation / developmental process

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