Cardiopharyngeal deconstruction and ancestral tunicate sessility

A key problem in understanding chordate evolution has been the origin of sessility of ascidians, and whether the appendicularian free-living style represents a primitive or derived condition of tunicates. To address this problem, we performed comprehensive developmental and genomic comparative analyses of the cardiopharyngeal gene regulatory network (GRN) between appendicularians and ascidians. Our results reveal that the cardiopharyngeal GRN has suffered a process of evolutionary deconstruction with massive ancestral losses of genes (Mesp, Ets1/2, Gata4/5/6, Mek1/2, Tbx1/10, and RA- and FGF-signaling related genes) and subfunctions (e.g. FoxF, Islet, Ebf, Mrf, Dach and Bmp signaling). These losses have led to the deconstruction of two modules of the cardiopharyngeal GRN that in ascidians are related to early and late multipotent state cells involved in lineage fate determination towards first and secondary heart fields, and siphon muscle. Our results allow us to propose an evolutionary scenario, in which the evolutionary deconstruction of the cardiopharyngeal GRN has had an adaptive impact on the acceleration of the developmental cardiac program, the redesign of the cardiac architecture into an open-wide laminar structure, and the loss of pharyngeal muscle. Our findings, therefore, provide evidence supporting that the ancestral tunicate had a sessile ascidian-like lifestyle, and points to the deconstruction of the cardiopharyngeal GRN in appendicularians as a key event that facilitated the evolution of their pelagic free-living style connected to the innovation of the house.

From heart-forming region to ballooning chambers

This chapter describes the formation of the adult four-chambered heart from the precardiac mesodermal cells. The precardiac mesoderm develops into a linear heart tube by the process of folding. The subsequent increase in size of the heart by the addition of precursor cells derived from the first and second heart fields is discussed. For the sake of clarity, the chapter describes the addition of precursor cells to the inflow and outflow, separately. Next, the formation of the ventricular chambers with respect to ballooning and differentiation into a compact and trabecular layer is discussed. Finally, the formation of the septa in the heart tube is described, creating the adult four-chambered heart.

The developmental origin of myocardium at the venous pole of the heart

The focus of this chapter is an evaluation of the developmental origin of the myocardial component of the venous pole. The venous pole has a complex morphological architecture, reflecting its embryological and evolutionary development from several component parts. We describe the developmental changes observed in the architecture of the inflow of the heart and the large vessels that drain into the venous pole. As the formation of the proepicardium and the epicardial-derived cells are intimately connected to the forming inflow, this topic will also be covered. We compare the development of the inflow in chicken, mouse, and human. We then review the results obtained using the two-component genetic mouse system Cre-LoxP with respect to the myocardial components added to the forming cardiac inflow. These data are discussed within the now discriminated first, second, and third heart fields.

Cardiac fields and myocardial cell lineages

We focus on the origin of myocardial cells in the first and second heart fields in splanchnic mesoderm in the early embryo. Genetic lineage tracing using Cre recombinase activated conditional reporter genes has made a major contribution to our understanding of cardiac progenitor cells and will be discussed together with other experimental approaches to analysing cell lineages at the clonal level. Interactions between myocardial, epicardial and endocardial lineages are essential for coordinated function and homeostasis of the normal heart. Perturbation of heart field development and myocardial lineage contributions to the heart through developmental or acquired pathologies results in and modulates the progression of cardiac disease. Understanding the origin of myocardial lineages during embryonic development and how they converge to generate an integrated heart is thus a major biomedical objective. Furthermore, reactivation of developmental programmes is likely to be of major importance in strategies aimed at repair of the damaged heart.