Gene Duplication, Co-Option and Recruitment during the Origin of the Vertebrate Brain from the Invertebrate Chordate Brain

Abstract

The brain of the basal chordate amphioxus has been compared to the vertebrate diencephalic forebrain, midbrain, hindbrain and spinal cord on the basis of the cell architecture from serial electron micrographs and patterns of developmental gene expression. In addition, genes specifying the neural plate and neural plate border as well as Gbx and Otx, that position the midbrain/hindbrain boundary (MHB), are expressed in comparable patterns in amphioxus and vertebrates. However, migratory neural crest is lacking in amphioxus, and although it has homologs of the genes that specify neural crest, they are not expressed at the edges of the amphioxus neural plate. Similarly, amphioxus has the genes that specify organizer properties of the MHB, but they are not expressed at the Gbx/Otx boundary as in vertebrates. Thus, the genetic machinery that created migratory neural crest and an MHB organizer was present in the ancestral chordate, but only co-opted for these new roles in vertebrates. Analyses with the amphioxus genome project strongly support the idea of two rounds of whole genome duplication with subsequent gene losses in the vertebrate lineage. Duplicates of developmental genes were preferentially retained. Although some genes apparently acquired roles in neural crest prior to these genome duplications, other key genes (e.g., FoxD3 in neural crest and Wnt1 at the MHB) were recruited into the respective gene networks after one or both genome duplications, suggesting that such an expansion of the genetic toolkit was critical for the evolution of these structures. The toolkit has also increased by alternative splicing. Contrary to the general rule, for at least one gene family with key roles in neural crest and the MHB, namely Pax genes, alternative splicing has not decreased subsequent to gene duplication. Thus, vertebrates have a much larger number of proteins available for mediating new functions in these tissues. The creation of new splice forms typically changes protein structure more than evolution of the protein after gene duplication. The functions of particular isoforms of key proteins expressed at the MHB and in neural crest have only just begun to be studied. Their roles in modulating gene networks may turn out to rival gene duplication for facilitating the evolution of structures such as neural crest and the MHB.

An anterior signaling center patterns and sizes the anterior neuroectoderm of the sea urchin embryo

“…For many years it was thought that anterior signaling centers were a vertebrate invention that led to the more complex territorial specification and morphogenetic processes of vertebrate forebrain/ eye field development (Holland and Short, 2008;Pani et al, 2012). This study, as well as recent studies in invertebrate chordate amphioxus and ambulacrarian hemichordate embryos (Onai et al, 2012;Pani et al, 2012), challenge this idea.…”

Evolutionary functional analysis and molecular regulation of the ZEB transcription factors

“…These findings are in agreement with the concept that a major phase of gene duplication occurred close to vertebrate origins. In other words, vertebrates possess a large repertoire of genes that can be used to mediate new functions during development and adult life stages [23]. Together with the Cephalochordata and the Urochordata, the Vertebrata form the phylum of the Chordata.…”

Immune and Nervous Systems: More Than Just a Superficial Similarity?

“…By developing specificity for particular ligand-coreceptor combinations, different types of cells can utilize similar molecular language (i.e., RET signaling), but still retain their individuality. The same could be said about different lineage cells utilizing different members of the gene family that encode PAX (Holland and Short, 2008;Ransohoff, 2009;Rothenberg and Pant, 2004) or the chemokine-chemokine receptor system (Ransohoff, 2009).…”