Patterning of a telencephalon-like region in the adult brain of amphioxus
Èlia Benito‐GutiérrezManuel StemmerSilvia D. RohrLaura SchuhmacherJocelyn L.Y. TangAleksandra MarconiGáspár JékelyDetlev Arendt
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ABSTRACT The evolutionary origin of the vertebrate telencephalon remains unsolved. A major challenge has been the identification of homologous brain parts in invertebrate chordates. Here we report evidence for a telencephalic region in the brain of amphioxus, the most basally branching invertebrate chordate. This region is characterised, like its vertebrate counterpart, by the combined expression of the telencephalic markers FoxG1, Emx and Lhx2/9 . It is located at the anterior neural border and dorsal-ventrally patterned, as in vertebrates, by the antagonistic expression of Pax4/6 and Nkx2.1 , and a ventral Hh signal. This part of the brain develops only after metamorphosis via sustained proliferation of neuronal progenitors at the ventricular zone. This is concomitant with a massive expansion of late differentiating neuronal types as revealed by neuropeptide and neurotransmitter profiling. Overall, our results suggest that the adult amphioxus brain shows remarkable similarities to the vertebrate embryonic brain, thus providing a key missing link in understanding the invertebrate-to-vertebrate transition in chordate brain evolution.Keywords:
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Genomic analysis has upended chordate phylogeny, placing the tunicates as the sister group to the vertebrates. This taxonomic rearrangement raises questions about the emergence of a tunicate/vertebrate ancestor. Characterization of developmental genes uniquely shared by tunicates and vertebrates is one promising approach for deciphering developmental shifts underlying acquisition of novel, ancestral traits. The matrix glycoprotein Fibronectin (FN) has long been considered a vertebrate-specific gene, playing a major instructive role in vertebrate embryonic development. However, the recent computational prediction of an orthologous "vertebrate-like" Fn gene in the genome of a tunicate, Ciona savignyi, challenges this viewpoint suggesting that Fn may have arisen in the shared tunicate/vertebrate ancestor. Here we verify the presence of a tunicate Fn ortholog. Transgenic reporter analysis was used to characterize a Ciona Fn enhancer driving expression in the notochord. Targeted knockdown in the notochord lineage indicates that FN is required for proper convergent extension. These findings suggest that acquisition of Fn was associated with altered notochord morphogenesis in the vertebrate/tunicate ancestor.
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The appendicularian urochordate Oikopleura dioica retains a free-swimming chordate body plan throughout life, in contrast to ascidian urochordates, whose metamorphosis to a sessile adult form involves the loss of chordate structures such as the notochord and dorsal nerve cord. Development to adult stages in Oikopleura involves a lengthening of the tail and notochord and an elaboration of the repertoire of tail movements. To investigate the cellular basis for this lengthening, we have used confocal microscopy and BrdU labeling to examine the development of the Oikopleura notochord from hatching through adult stages. We show that as the notochord undergoes the typical urochordate transition from a stacked row of cells to a tubular structure, cell number begins to increase. Addition of new notochord cells continues into adulthood, multiplying the larval complement of 20 cells by about 8-fold by the third day of life. In parallel, the notochord lengthens by about 4-fold. BrdU incorporation and a cell-cycle marker confirm that notochord cells continue to proliferate well into adulthood. The extensive postlarval proliferation of notochord cells, together with their arrangement in four circumferentially distributed longitudinal rows, presumably provides the Oikopleura tail with the necessary mechanical support for the complex movements exhibited at adult stages.
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Urochordates are the closest relatives of vertebrates and at the larval stage, possess a characteristic bilateral chordate body plan. In vertebrates, the genes that orchestrate embryonic patterning are in part regulated by highly conserved non-coding elements (CNEs), yet these elements have not been identified in urochordate genomes. Consequently the evolution of the cis-regulatory code for urochordate development remains largely uncharacterised. Here, we use genome-wide comparisons between C. intestinalis and C. savignyi to identify putative urochordate cis-regulatory sequences. Ciona conserved non-coding elements (ciCNEs) are associated with largely the same key regulatory genes as vertebrate CNEs. Furthermore, some of the tested ciCNEs are able to activate reporter gene expression in both zebrafish and Ciona embryos, in a pattern that at least partially overlaps that of the gene they associate with, despite the absence of sequence identity. We also show that the ability of a ciCNE to up-regulate gene expression in vertebrate embryos can in some cases be localised to short sub-sequences, suggesting that functional cross-talk may be defined by small regions of ancestral regulatory logic, although functional sub-sequences may also be dispersed across the whole element. We conclude that the structure and organisation of cis-regulatory modules is very different between vertebrates and urochordates, reflecting their separate evolutionary histories. However, functional cross-talk still exists because the same repertoire of transcription factors has likely guided their parallel evolution, exploiting similar sets of binding sites but in different combinations.
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Abstract Metamorphosis displays a striking diversity in chordates, a deuterostome phylum that comprises vertebrates, urochordates (tunicates), and cephalochordates (amphioxus). In anuran amphibians, the tadpole loses its tail, develops limbs, and undergoes profound changes at the behavioral, physiological, biochemical, and ecological levels. In ascidian tunicates, the tail is lost and the head tissues are drastically remodeled into the adult animal, whereas in amphioxus, the highly asymmetric larva transforms into a relatively symmetric adult. This wide diversity has led to the proposal that metamorphosis evolved several times independently in the different chordate lineages during evolution. However, the molecular mechanisms involved in metamorphosis are largely unknown outside amphibians and teleost fishes, in which metamorphosis is regulated by the thyroid hormones (TH) T 3 and T 4 binding to their receptors (thyroid hormone receptors). In this review, we compare metamorphosis in chordates and then propose a unifying definition of the larva‐to‐adult transition, based on the conservation of the role of THs and some of their derivatives as the main regulators of metamorphosis. According to this definition, all chordates (if not, all deuterostomes) have a homologous metamorphosis stage during their postembryonic development. The intensity and the nature of the morphological remodeling varies extensively among taxa, from drastic remodeling like in some ascidians or amphibians to more subtle events, as in mammals. genesis 46:657–672, 2008. © 2008 Wiley‐Liss, Inc.
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ABSTRACT The evolutionary origin of the vertebrate telencephalon remains unsolved. A major challenge has been the identification of homologous brain parts in invertebrate chordates. Here we report evidence for a telencephalic region in the brain of amphioxus, the most basally branching invertebrate chordate. This region is characterised, like its vertebrate counterpart, by the combined expression of the telencephalic markers FoxG1, Emx and Lhx2/9 . It is located at the anterior neural border and dorsal-ventrally patterned, as in vertebrates, by the antagonistic expression of Pax4/6 and Nkx2.1 , and a ventral Hh signal. This part of the brain develops only after metamorphosis via sustained proliferation of neuronal progenitors at the ventricular zone. This is concomitant with a massive expansion of late differentiating neuronal types as revealed by neuropeptide and neurotransmitter profiling. Overall, our results suggest that the adult amphioxus brain shows remarkable similarities to the vertebrate embryonic brain, thus providing a key missing link in understanding the invertebrate-to-vertebrate transition in chordate brain evolution.
Chordate
Ganglionic eminence
Notochord
Cite
Citations (12)