Patterning the early Xenopus embryo

Developmental biology teachers use the example of the frog embryo to introduce young scientists to the wonders of vertebrate development, and to pose the crucial question, 'How does a ball of cells become an exquisitely patterned embryo?'. Classical embryologists also recognized the power of the amphibian model and used extirpation and explant studies to explore early embryo polarity and to define signaling centers in blastula and gastrula stage embryos. This review revisits these early stages of Xenopus development and summarizes the recent explosion of information on the intrinsic and extrinsic factors that are responsible for the first phases of embryonic patterning.     

Patterning of angiogenesis in the zebrafish embryo

Little is known about how vascular patterns are generated in the embryo. The vasculature of the zebrafish trunk has an extremely regular pattern. One intersegmental vessel (ISV) sprouts from the aorta, runs between each pair of somites, and connects to the dorsal longitudinal anastomotic vessel (DLAV). We now define the cellular origins, migratory paths and cell fates that generate these metameric vessels of the trunk. Additionally, by a genetic screen we define one gene, out of bounds (obd), that constrains this angiogenic growth to a specific path. We have performed lineage analysis, using laser activation of a caged dye and mosaic construction to determine the origin of cells that constitute the ISV. Individual angioblasts destined for the ISVs arise from the lateral posterior mesoderm (LPM), and migrate to the dorsal aorta, from where they migrate between somites to their final position in the ISVs and dorsal longitudinal anastomotic vessel (DLAV). Cells of each ISV leave the aorta only between the ventral regions of two adjacent somites, and migrate dorsally to assume one of three ISV cell fates. Most dorsal is a T-shaped cell, based in the DLAV and branching ventrally; the second constitutes a connecting cell; and the third an inverted T-shaped cell, based in the aorta and branching dorsally. The ISV remains between somites during its ventral course, but changes to run mid-somite dorsally. This suggests that the pattern of ISV growth ventrally and dorsally is guided by different cues. We have also performed an ENU mutagenesis screen of 750 mutagenized genomes and identified one mutation, obd that disrupts this pattern. In obd mutant embryos, ISVs sprout precociously at abnormal sites and migrate anomalously in the vicinity of ventral somite. The dorsal extent of the ISV is less perturbed. Precocious sprouting can be inhibited in a VEGF morphant, but the anomalous site of origin of obd ISVs remains. In mosaic embryos, obd somite causes adjacent wild-type endothelial cells to assume the anomalous ISV pattern of obd embryos. Thus, the launching position of the new sprout and its initial trajectory are directed by inhibitory signals from ventral somites. Zebrafish ISVs are a tractable system for defining the origins and fates of vessels, and for dissecting elements that govern patterns of vessel growth.     

Patterning lessons from a dorsalized embryo

A paper by Nunes da Fonseca and colleagues in this issue of Developmental Cell shows that, to pattern its dorsoventral axis, the beetle Tribolium utilizes many of the same genes used in flies, but in very different ways: rather than relying on maternal information, it uses Dorsal and Dpp as part of two coordinated ancestral self-organized systems.     

Patterning the female side of Arabidopsis: the importance of hormones

The study of floral organ development has been a driving force in plant developmental biology research for the last two decades, and there is now an enormous wealth of information about the genetic networks underlying the specification of floral organ identity and the acquisition of its final morphology and function. These and parallel studies on leaf morphogenesis and development have made evident the common evolutionary origin of all plant lateral organs and the recurrent use of variations in the regulatory circuits involved in the shaping of leaves and flowers. This review summarizes the latest progress on the study of the development of the gynoecium, the female reproductive organ of the flower, stressing the connections with the developmental programme of leaf morphogenesis, and highlighting the common role of hormonal cues in these processes.     

Patterning the embryo in higher plants: Emerging pathways and challenges

Embryogenesis, which establishes the basic body plan for the post-embryonic organs after stereotyped cell divisions, initiates the first step of the plant life cycle. Studies in the last two decades indicate that embryogenesis is a precisely controlled process, and any defect would result in abnormalities. Here we discuss the recent progresses, with a focus on the cellular pathways governing early embryogenesis in the model species Arabidopsis.     

Plasma Membrane Domain Patterning and Self-Reinforcing Polarity in Arabidopsis

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Patterning the C. elegans embryo: moving beyond the cell lineage.

The Caenorhabditis elegans embryo undergoes a series of stereotyped cell cleavages that generates the organs and tissues necessary for an animal to survive. Here we review two models of embryonic patterning, one that is lineage-based, and one that focuses on domains of organ and tissue precursors. Our evolving view of C. elegans embryogenesis suggests that this animal develops by mechanisms that are qualitatively similar to those used by other animals.     

A PHABULOSA-Controlled Genetic Pathway Regulates Ground Tissue Patterning in the Arabidopsis Root

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Patterning of the embryo: the first spatial decisions in the life of a mouse

Although in most species the polarity of the embryo takes its roots from the spatial patterning of the egg, mammals were viewed as an exception. This was because the anteroposterior polarity of the mouse embryo could not be seen until gastrulation, and no developmental cues were known that could define polarity at earlier stages. Why should we now re-consider this view? While mechanisms of axis formation in mammals could, in principle, be unique, the evolutionary conservation of numerous other developmental processes raises the question of why mammals would have evolved a different way or timing of organising their embryonic polarity. Indeed, recent evidence shows that well before the onset of gastrulation, the mouse embryo initiates asymmetric patterns of gene expression in its visceral endoderm. Although this extra-embryonic tissue does not contribute to the body itself, it is involved in axis formation. Other recent work has revealed that spatial distribution of cells in the visceral endoderm can be traced back to polarity present at the blastocyst stage. These insights have raised the possibility that embryonic polarity might also originate early during development of mammalian embryos. Indeed it now appears that there are at least two spatial cues that operate in the mouse egg to shape polarity of the blastocyst. One of these is at the animal pole, which is defined by the site of female meiosis, and another is associated with the position of sperm entry. In this review I discuss these recent findings, which have led to the recognition that mouse embryos initiate development of their polarity at the earliest stages of their life. This novel perspective raises questions about the nature of cellular and molecular mechanisms that could convert developmental cues in the zygote to axes of the blastocyst, and hence into polarity of the post-implantation embryo. It also brings to light the need to understand how such mechanisms could enable early mouse development to be so regulative.     

A Dynamic Model for Stem Cell Homeostasis and Patterning in Arabidopsis Meristems

Plants maintain stem cells in their meristems as a source for new undifferentiated cells throughout their life. Meristems are small groups of cells that provide the microenvironment that allows stem cells to prosper. Homeostasis of a stem cell domain within a growing meristem is achieved by signalling between stem cells and surrounding cells. We have here simulated the origin and maintenance of a defined stem cell domain at the tip of Arabidopsis shoot meristems, based on the assumption that meristems are self-organizing systems. The model comprises two coupled feedback regulated genetic systems that control stem cell behaviour. Using a minimal set of spatial parameters, the mathematical model allows to predict the generation, shape and size of the stem cell domain, and the underlying organizing centre. We use the model to explore the parameter space that allows stem cell maintenance, and to simulate the consequences of mutations, gene misexpression and cell ablations.