Preface. Developmental Morphodynamics - bridging the gap between the genome and embryo physics.

We, the Guest Editors of this Special Issue of The International Journal of Developmental Biology, are two older embryologists, who are trying to bridge the current chasm between Entwicklungsmechanic, the developmental mechanics of our embryogenesis forefathers, and the modern movement of molecular developmental biology. Our rallying cry is that of Wilhelm His: "To think that heredity will build organic beings without mechanical means is a piece of unscientific mysticism" (His, 1888). Until recently, this claim appeared to us to fall on the somewhat deaf ears of molecular developmental biologists. Yet, the world is still one, and both physics and chemistry obviously have their place in embryogenesis. Indeed, at the molecular level, membrane proteins which are mechanoreceptors and motor molecules may begin to point the way. Here, we and our colleagues will make the case for a more equitable consideration of molecules and mechanics.     

Morphogenesis as a macroscopic self-organizing process

We start from reviewing different epistemological constructions used for explaining morphogenesis. Among them, we explore the explanatory power of a law-centered approach which includes top-down causation and the basic concepts of a self-organization theory. Within such a framework, we discuss the morphomechanical models based upon the presumption of feedbacks between mechanical stresses imposed onto a given embryo part from outside and those generated within the latter as a kind of active response. A number of elementary morphogenetic events demonstrating that these feedbacks are directed towards hyper-restoration (restoration with an overshoot) of the initial state of mechanical stresses are described. Moreover, we show that these reactions are bound together into the larger scale feedbacks. That permits to suggest a reconstruction of morphogenetic successions in early Metazoan development concentrated around two main archetypes distinguished by the blastopores geometry. The perspectives of applying the same approach to cell differentiation are outlined. By discussing the problem of positional information we suggest that the developmental pathway of a given embryo part depends upon its preceded deformations and the corresponding mechanical stresses rather than upon its static position at any moment of development.     

Studies of morphogenesis at the Department of Embryology, Moscow State University: Towards understanding the dynamic architecture of development

This is a review of studies on morphogenesis carried out at the Department of Embryology, Moscow State University, over the past 30 years. The main direction of studies has been to reveal and describe the properties of self-organizing fields of mechanical stresses in developing embryos.     

Formative capacities of mechanically stressed networks: developmental and evolutionary implications.

We present a biomechanical model of morphogenesis highlighting the extensive formative capacities of stressed networks with a very simple initial geometry. They consist of a restricted number of kinematically independent elements exerting a pressure to each other and increasing thus the local curvatures. The pressure is applied as a series of periodic impulses and is opposed by a constant quasi-elastic resistance force. Single elements can be also regarded as the half wave-lengths of the undulations determined by the mechanical properties of a given body. All of the model parameters are assumed to be evenly spread throughout a body (no prepatterns are implied). On the other hand, the model parameters can be associated with genetic factors. Thus, our model relates to as yet unsolved problem of genetic regulation of shape formation. We classify the modeled shapes according to their symmetry orders and compare them with the ancient Echinodermata and with Arthropods. Possible evolutionary and developmental implications are discussed.     

Relocations of cell convergence sites and formation of pharyngula-like shapes in mechanically relaxed <Emphasis Type="Italic">Xenopus</Emphasis> embryos

Influence of the relaxation of mechanical tensions upon collective cell movements, shape formation, and expression patterns of tissue-specific genes has been studied in Xenopus laevis embryos. We show that the local relaxation of tensile stresses within the suprablastoporal area (SBA) performed at the early-midgastrula stage leads to a complete arrest of normal convergent cell intercalation towards the dorsal midline. As a result, SBA either remains nondeformed or protrudes a strip of cells migrating ventralwards along one of the lateral lips of the opened blastopore. Already, few minutes later, the tissues in the ventral lip vicinity undergo abnormal transversal contraction/longitudinal extension resulting in the abnormal cell convergence toward ventral (rather than dorsal) embryo midline. Within a day, the dorsally relaxed embryos acquire pharyngula-like shapes and often possess tail-like protrusions. Their antero-posterior and dorso-ventral polarity, as well as expression patterns of pan-neural (Sox3), muscular cardiac actin, and forebrain (Otx2) genes substantially deviate from the normal ones. We suggest that normal gastrulation is permanently controlled by mechanical stresses within the blastopore circumference. The role of tissue tensions in regulating collective cell movements and creating pharyngula-like shapes are discussed.     

Mechanodependent cell movements in the axial rudiments of <Emphasis Type="Italic">Xenopus</Emphasis> gastrulae

Sandwich explants of the suprablastoporal area of Xenopus early-mid gastrula and same stages of entire embryos were stretched with two needles perpendicular to the direction of natural elongation of the axial rudiments. The changes in the embryonic shape and histological structure were monitored as well as the arrangement of descendants of one of dorsal blastomers labeled with fluorescein-dextran at the 16-cell stage. A substantial fraction of stretched explants reoriented along the applied stretch direction. The arrangement dynamics of fluorescein-dextran-labeled cells and explant shape demonstrate that this is an active response based on convergent intercalation of cells induced by stretching. Stretched gastrulae demonstrated arrested gastrulation, dorsoventral extension of the blastopore, and ventral flow of labeled cells towards the lateral lips of the blastopore, which was also mediated by convergent intercalation and tensotaxis. The obtained data are discussed in terms of the hypothesis of mechanical stress hyper-restoration.     

X-ray microanalysis of ion contents in vacuoles and cytoplasm of the growing tips of a hydroid polyp as related to osmotic changes and growth pulsations

Growth pulsations (GP) in hydroid polyps are associated with changes in vacuolar patterns which can be imitated by altering external osmolarity. With the use of X-ray spectroscopy we measured the elemental contents in the vacuoles and cytoplasm of the growing tips of a hydroid polyp, Podocoryne carnea, under various tonicity conditions. Under hypertonic condition which arrested the samples at the retraction phase of normal GP, the elemental content within the vacuolar compartment appeared to be similar to that of the external medium, confirming our previous conclusion about the dehermetization of the vacuolar compartment under these conditions. Under hypotonical condition which arrested samples at the extension GP phase (vacuoles isolated) element ratio data displayed an obvious bimodality. At least one of the data groups could be characterized by a significant increase in the concentrations of sodium and potassium, as related to Cl, Ca and Mg, and in comparison to the same ratios in hypotonical samples and those in the external medium. We suggest that under hypotonical conditions the isolated vacuolar compartment is formed by influx of sodium and potassium ions. These cations are accompanied by anions other than chloride. Potassium appears to be transferred into the vacuoles from the cytoplasm while the sodium derives from the external environment.     

Morphogenetic fields: outlining the alternatives and enlarging the context.

Several alternative properties which we define as deterministic or field ones are formulated and analyzed in their relations to the realms of morphogenesis and biophoton emission. In spite of all the differences between these two groups of events both of them share the properties of non-additivity, delocalization, self-focusing and several others which we relate to the field phenomena. To a large extent, the field properties of the biological systems are associated with a set of oscillations of different time periods. We suggest that even such deterministic events as, for example, a ligand-receptor coupling are acting, within an activated cell, as the switches and/or modulators of its field properties.