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Evolution of the craniate brain : patterning and regionalisation of the lamprey developing forebrain.

Abstract : Lampreys are becoming increasingly popular in evolutionary developmental biology, due to their phylogenetic position. They provide insights into craniate ancestral characteristics, but also into the emergence of novelties at the important cyclostome/gnathostome evolutionary split (Kuratani et al.,2002).
This work was focused on the study of the genetic specification and organisation of the embryonic lamprey brain. By RT-PCR cloning and in situ hybridisation we were able to isolate and study the expression pattern of genes from the LIM-homeobox (Lhx), Pax and Hedgehog families. The main results are as follows: (1) Lhx and Pax genes reveal a strikingly similar forebrain and hindbrain patterning between cyclostomes and gnathostomes; some important differences are nevertheless observed, especially at the level of the telencephalon, a region where major changes took place at the cyclostome/- gnathostome division; (2) the interpretation of the expression pattern of Lhx genes shows that the lamprey forebrain presents a clear prosomeric organisation, which is thus a truly craniate character; (3) analysis of the LfHh gene expression reveals the possible molecular origin of this neuromeric brain pattern (Osorio et al., 2005); (4) finally, Lhx gene expression persists through the larval (non-embryonic) period, making these genes useful markers to follow brain development and morphogenesis (Osorio et al., 2006).
This brain organisation is restricted to gnathostomes: in amphioxus and ascidians, where the expression of Hh is absent from the anteriormost part of the neural tube, no neuromeres are observed. Importantly, Hh is not expressed in the embryonic lamprey ventral telencephalon, and Nkx2.1, a marker of the pallidal subdivision of the gnathostome-specific subpallium, is not expressed in the embryonic lamprey subpallium (Ogasawara et al., 2001; Osorio et al., 2005; Uchida et al., 2003). This difference points out the possible role of the Hh ventral midline signalling as a powerful motor of forebrain evolution.
We next sought to investigate the origin of these differences in the light of the molecular evolution of the Hedgehog multigene family. It is likely that the chordate ancestor possessed a unique Hh gene. The cephalochordate amphioxushas still a single Hh gene, while there are two in ascidians, originated by a urochordate-specific duplication. There are three groups of Hh genes in gnathostomes (Sonic, Indian and Desert).
We have screened a cosmid genomic DNA library of L. fluviatilis aiming at identifying cosmids containing the Hh gene. The results strongly suggest the existence of two Hedgehog genes in lamprey. A preliminary phylogenetic analysis suggests an independent duplication of the lamprey Hedgehog genes within the Sonic/Indian group. These findings open a new vision on the evolution of this gene family within chordates.
Finally, with the purpose of studying the role of changes in gene organization and control of gene expression in the evolution of the chordate brain, we have also isolated the Lhx9 gene from a dogfish (Scyliorhinus canicula) BAC genomic library.
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Submitted on : Friday, September 21, 2007 - 6:16:30 PM
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Joana Vaz Pato Osorio, Joana Osório. Evolution of the craniate brain : patterning and regionalisation of the lamprey developing forebrain.. Neurons and Cognition [q-bio.NC]. Université Paris Sud - Paris XI, 2007. English. ⟨tel-00174226⟩



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