Nodal signaling and the evolution of deuterostome gastrulation

Abstract

Chordates, including vertebrates, evolved within a group of animals called the deuterostomes. All holoblastic deuterostomes gastrulate at the vegetal pole and the blastopore becomes the anus, while a mouth is formed at the anterior or to the oral side. Nodal is a member of the TGF-␤ superfamily of signaling molecules that are important in signaling between cells during many embryonic processes in vertebrate embryos. Nodal has also been found in other invertebrate deuterostomes, such as ascidians and sea urchins, but, so far, is missing in protostomes. Nodal has been shown to be particularly important in determining left-right asymmetries in vertebrate embryos, but less information is available for its developmental role in the invertebrate deuterostomes. We review gastrulation in the deuterostomes, then examine nodal expression early during mesoderm formation and later during the establishment of asymmetries in both vertebrates and invertebrates. Nodal is expressed asymmetrically on the left side in chordates and on the presumptive oral side of the embryo in echinoid echinoderms. The expression of nodal is in different germ layers in embryos of different phyla. Expression is in the ectoderm in most of the invertebrate deuterostomes, and in the mesoderm in vertebrates. We summarize the work that has been published to date, especially nodal expression in the invertebrate deuterostomes, and suggest future experiments to better understand the evolution of nodal signaling and deuterostome gastrulation. Developmental Dynamics 234:269 -278, 2005.

Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives

“…Nodal is so far one of the few described deuterostome-specific genes, evolving from the duplication of a BMP-like ancestor (Duboc et al 2004;Chea et al 2005). In deuterostomes, there is early nodal embryonic expression (not shown), but later nodal signalling results in left-right asymmetry of certain organs in bilateral embryos ( figure 3).…”

“…In deuterostomes, there is early nodal embryonic expression (not shown), but later nodal signalling results in left-right asymmetry of certain organs in bilateral embryos ( figure 3). In all chordates, later nodal expression is on the left side during development, specifying asymmetry (Chea et al 2005). However, in sea urchins, nodal is expressed on the right side at the later period, opposite of adult rudiment formation (Duboc et al 2004(Duboc et al , 2005.…”

“…Traditionally, the group was recognized on the basis of a shared embryonic development pattern: gastrulation occurs at the vegetal pole and the blastopore becomes the anus, while the mouth forms secondarily (Chea et al 2005). Analysis of molecular data has consistently found the deuterostome grouping, generally with high levels of support Philippe et al 2005;Delsuc et al 2006).…”

Retinoic acid signaling in development: Tissue‐specific functions and evolutionary origins

“…RA signaling probably controls expression of genes involved in setting up left/right asymmetry in the early vertebrate embryo, such as lefty, pitx, and nodal (Chazaud et al, 1999;Tsukui et al, 1999). In invertebrate chordates, as in other invertebrate deuterostomes, the establishment of left/right asymmetry probably involves the same gene hierarchy as in vertebrates (Chea et al, 2005;Duboc et al, 2004Duboc et al, , 2005. For example, as in vertebrates, homologs of shh, pitx, and nodal are all expressed asymmetrically during amphioxus development (Schubert et al, 2005;Yu et al, 2007).…”

Nutritional endoderm in a direct developing frog: A potential parallel to the evolution of the amniote egg

“…Vigorous attempts have been made to use phylogenetic methods to decide between these hypotheses, but these attempts have not produced a resolution (Laurin and Reisz, 1997;Wilkinson et al, 2002;Laurin, 2005). On the other hand, there is general consensus on biological and phylogenetic grounds that the eggs of the original tetrapods were much like those of extant amphibians and cleaved holoblastically (Romer, 1957;Goin and Goin, 1962;Carroll, 1969Carroll, , 1970Elinson, 1987Elinson, , 1989Collazo et al, 1994;Packard and Seymour, 1997;Arendt and Nü bler-Jung, 1999;Elinson and Beckham, 2002;Chea et al, 2005). A transition to meroblastic cleavage would be one of the conditions, along with provision for gas exchange, which permitted the great increase in yolk content and egg size, found in the amniotes.…”