Lamprey Dlx genes and early vertebrate evolution

Abstract

Gnathostome vertebrates have multiple members of the Dlx family of transcription factors that are expressed during the development of several tissues considered to be vertebrate synapomorphies, including the forebrain, cranial neural crest, placodes, and pharyngeal arches. The Dlx gene family thus presents an ideal system in which to examine the relationship between gene duplication and morphological innovation during vertebrate evolution. Toward this end, we have cloned Dlx genes from the lamprey Petromyzon marinus, an agnathan vertebrate that occupies a critical phylogenetic position between cephalochordates and gnathostomes. We have identified four Dlx genes in P. marinus, whose orthology with gnathostome Dlx genes provides a model for how this gene family evolved in the vertebrate lineage. Differential expression of these lamprey Dlx genes in the forebrain, cranial neural crest, pharyngeal arches, and sensory placodes of lamprey embryos provides insight into the developmental evolution of these structures as well as a model of regulatory evolution after Dlx gene duplication events.

Jaw transformation with gain of symmetry after Dlx5/Dlx6 inactivation: Mirror of the past?

“…Our findings might imply, more generally, that Dlx genes were needed to allow asymmetry when required by the rise of complex anatomical structures during evolution. Our data reinforce the concept, already present in the literature that Dlx genes are associated with the appearance of morphological novelties in vertebrates (Neidert et al, 2001).…”

“…Based on sequencing comparison, it is thought that during the evolution of chordates an initial gene duplication occurred, followed by several cluster duplications and selective gene losses (Stock et al, 1996;Ruddle, 1997;Zerucha and Ekker, 2000). Dll homologs have been isolated from vertebrate species like lamprey, zebrafish, newt, Xenopus, mouse, and human (see Neidert et al, 2001, and references therein). They constitute a highly conserved family of homeobox genes, which are thought to act as transcription factors.…”

Development of the viscerocranial skeleton during embryogenesis of the sea lamprey,Petromyzon Marinus

“…Nevertheless, these differences suggest that the dorsal and ventral elements of the branchial basket may consist of two separate embryonic components. In jawed vertebrates, the nested expression of dlx genes is important for establishing dorsoventral (proximodistal) polarity in branchial arches (Panganiban and Rubenstein, 2002;Depew et al, 2005), although Langeland and his colleagues (Neidert et al, 2001) reported no dorsoventral patterning of dlx expression in is attached to the parachordal cartilage lateral to the notochord. Remaining caudal skeletal rods (PA4-9) attach to the subchordal cartilages on the ventral surface of the notochord.…”

Expression of the dlx gene family during formation of the cranial bones in the zebrafish (Danio rerio): Differential involvement in the visceral skeleton and braincase

“…In vertebrates, all Dlx genes except zebrafish dlx2b, are expressed in ectomesenchymal cells derived from the cranial neural crest (Dollé et al, 1992;Bulfone et al, 1993;Akimenko et al, 1994;Robinson and Mahon, 1994;Simeone et al, 1994;Qiu et al, 1997;Yang et al, 1998;Davideau et al, 1999;Myojin et al, 2001;Neidert et al, 2001). The migratory neural crest cells populate the branchial arches, which in turn give rise to much of the craniofacial skeleton and connective tissue (Depew et al, 2002).…”

“…To account for the present complement of six mammalian Dlx genes, i.e., Dlx1, Dlx2, Dlx3, Dlx4 (formerly Dlx7), Dlx5, Dlx6, a tandem duplication of an ancestral Dlx gene has been proposed to have been followed by two rounds of genome duplication and a subsequent loss of one Dlx pair (Ellies et al, 1997;Neidert et al, 2001).…”