Evolutionary aspects of developmentally regulated helix-loop-helix transcription factors in striated muscle of jellyfish

Abstract

The function of basic helix-loop-helix (bHLH) proteins in cell differentiation was shown to be conserved from Drosophila to vertebrates, exemplified by the function of MyoD in striated muscle differentiation. In phylogeny striated muscle tissue appears first in jellyfish and the question of its evolutionary position is controversially discussed. For this reason we have studied the developmental role of myogenic bHLH genes in medusa development. Based on their dimerization ability, four genes of the bHLH family of transcription factors were isolated from the hydrozoan jellyfish Podocoryne carnea. While the proteins Id and Ash group with cognate family members from bilaterians, Net-like and JellyD1 could not be unequivocally classified. Id is expressed during the medusa budding process and in the adult medusa, Ash and Net-like are expressed in all life cycle stages from egg to adult medusa and JellyD1 is expressed in the blastula and gastrula stages, the planula larva, and in late medusa bud stages. The dimerization specificity, the expression pattern, and the conservation of two residues specific for a MyoD bHLH domain suggest that JellyD1 is related to an ancestral MyoD gene. Id, Net-like, and JellyD1 are either expressed in the entocodon or its derived tissues, the striated and smooth muscle of the bell. These findings strengthen the hypothesis that the entocodon is a mesoderm-like structure and that the common ancestor of Cnidaria and Bilateria was more complex in cell-type architecture and body organization than commonly thought.

A hedgehog homolog is involved in muscle formation and organization of Sepia officinalis (mollusca) mantle

“…In order to demonstrate that the cuttlefish mantle's muscle precursors derive from the external integument layer, we performed immunolocalization assays using an antibody raised against the muscular myogenic factor MyoD, which is specifically expressed in the muscular precursors in both vertebrates and invertebrates (Krause et al, 1992;Buckingham, 1994;Chen et al, 1994;Krause et al, 1994;Ontell et al, 1995;Misquitta and Paterson, 1999;Muller et al, 2003;Grimaldi et al, 2004c) together with an antibody raised against desmin, one of the earliest myogenic markers (Choi et al, 1990).…”

Basic leucine zipper transcription factors C/EBP and MafL in the hydrozoan jellyfish Podocoryne carnea

“…Unlike other cnidarians, Podocoryne carnea features a complete life cycle such that all aspects of cnidarian development are accessible. Molecular studies have revealed that a substantial part of the genetic machinery regulating vertebrate development is also present in the jellyfish, including genes for homeobox transcription factors (Yanze et al, 2001) and several basic helix-loop-helix transcription factors (Spring et al, 2000, Mü ller et al, 2003Seipel et al, 2004). Here, we describe candidate genes for the bzip transcription factors C/EBP and MafL.…”

“…The recent molecular analysis of a variety of developmental regulatory genes (Aerne et al, 1995;Spring et al, 2000Spring et al, , 2002Mü ller et al, 2003) indicate that the budding process can be viewed as a continuation of gastrulation, where larva formation concludes the first and bud formation the second phase. Schematic drawings of medusa development are included in Figures 5 and 6.…”

“…Because the entocodon cells are clearly separated from the ectoderm and endoderm by the formation of an extracellular matrix (Bö elsterli, 1977), they constitute a third germ layer (Boero et al, 1998). The entocodon produces the striated and smooth muscle of the bell through gene cascades comparable to those in the bilaterian mesodermates (Spring et al, 2000(Spring et al, , 2002Mü ller et al, 2003). Expression of both genes is absent in the young entocodon (Figs.…”

“…Similarly, the development of the striated and smooth muscle of the jellyfish bell is orchestrated by regulatory pathways comparable to those in the bilaterian mesodermates (Spring et al, 2000(Spring et al, , 2002Mü ller et al, 2003). In fact, a substantial part of the genetic machinery regulating vertebrate development is also present in the jellyfish, including genes for homeobox transcription factors (Yanze et al, 2001) and several basic helix-loop-helix transcription factors (Spring et al, 2000;Mü ller et al, 2003;Seipel et al, 2004). In evolutionary terms, the genetic machinery necessary to build the hypothetical common ancestor of Cnidaria and Bilateria, supposedly extant between 500 and 1,400 million years ago, contained a great variety of the regulators still in use to date.…”